The calcium ion and conserved water molecules in neuraminidases: Roles and implications for substrate binding

Internet Electronic Journal of Molecular Design

Volumn 7, Issue 5, 2008, Pages 97-113

  Yang, Gang ^a,b   Yang, Zhiwei ^a   Zu, Yuangang ^a   Wu, Xiaomin ^a   Fu, Yujie ^a  

^a NORTHEAST FORESTRY UNIVERSITY   (China)

^b DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

Author keywords

Active site; Calcium ion; Conserved water molecules; Neuraminidase; Substrate binding

Indexed keywords

ORTHOMYXOVIRIDAE;

EID: 57549112973     PISSN: None     EISSN: 15386414     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. E. Garman and G. Laver. Controlling Influenza by Inhibiting the Virus's Neuraminidase. Curr. Drug Targets. 2004, 5, 119-136.
2. A. Moscona. Neuraminidase Inhibitors for Influenza. New. Engl. J. Med. 2005, 353, 1363-1373.
3. J. R. Rupert, F. H. Lesley, J. S. David, J. C. Patrick, P.-L. Yi, B. G. Michael, J. H. Alan, J. G. Steven, and J. S. John. The Structure of H5N1 Avian Influenza Neuraminidase Suggests New Opportunities for Drug Design. Nature 2006, 443, 45-49.
4. P. Sears and C. H. Wong. Carbohydrate Mimetics: A New Strategy for Tackling the Problem of Carbohydrate-Mediated Biological Recognition. Angew. Chem. Int. Ed. 1999, 38, 2300-2324.
5. N. R. Taylor, A. Cleasby, O. Singh, T. Skarzynski, A. J. Wonacott, P. W. Smith, S. L. Sollis, P. D. Howes, P. C. Cherry, R. Bethell, P. Colman, and J. Varghese. Dihydropyrancarboxamides Related to Zanamivir: a New Series of Inhibitors of Influenza Virus Sialidases. 2. Crystallographic and Molecular Modeling Study of Complexes of 4-amino-4H-pyran-6-carboxamides and Sialidase from Influenza Virus Types A and B. J. Med. Chem. 1998, 41, 798-807.
6. J. N. Varghese, P. W. Smith, S. L. Sollis, T. J. Blick, A. Sahasrabudhe, J. L. Mc-Kimm-Breschin, and P. M. Colman. Drug Design Against a Shifting Target: a Structural Basis for Resistance to Inhibitors in a Variant of Influenza Virus Neuraminidase. Structure 1998, 6, 735-746.
7. Y. S. Babu, P. Chand, S. Bantia, P. Kotian, A. Dehghani, Y. El-Kattan, T. H. Lin, T. L. Hutchison, A. J. Elliott, C. D. Parker, S. L. Ananth, L. L. Horn, G. W. Laver, and J. A. Montgomery. BCX-1812 (RWJ-270201): Discovery of a Novel, Highly Potent, Orally Active, and Selective Influenza Neuraminidase Inhibitor Through Structure-based Drug Design. J. Med. Chem. 2000, 43, 3482-3486.
8. B. J. Smith, J. L. McKimm-Breshkin, M. McDonald, R. T. Fernley, J. N. Varghese, and P. M. Colman. Structural Studies of the Resistance of Influenza Virus Neuramindase to Inhibitors. J. Med. Chem. 2002, 45, 2207-2212.
9. C. W. Murray, C. A. Baxter and A. D. Frenkel. The Sensitivity of the Results of Molecular Docking to Induced Fit Effects: Application to Thrombin, Thermolysin and Neuraminidase. J. Comput. Aided Mol. Des. 1999, 13, 547-562.
10. X. Yi, Z. Guo, and F. M. Chu. Study on Molecular Mechanism and 3D-QSAR of Influenza Neuraminidase Inhibitors. Bioorg. Med. Chem. 2003, 11, 1465-1474.
11. M. C. Mann, T. Islam, J. C. Dyason, P. Florio, C. J. Trower, R. J. Thomson, and M. von Itzstein. Unsaturated N-acetyl-D-glucosaminuronic Acid Glycosides as Inhibitors of Influenza Virus Sialidase. Glycoconj J. 2006, 23, 127-133.
12. D. Platis, B. J. Smith, T. Huyton, and N. E. Labrou. Structure-guided Design of a Novel Class of Benzyl-sulfonate Inhibitors for Influenza Virus Neuraminidase. Biochem J. 2006, 399, 215-223.
13. C. Sun, X. Zhang, H. Huang, and P. Zhou. Synthesis and Evaluation of a New Deries of Substituted Acyl(thio)urea and Thiadiazolo [2,3-α] Pyrimidine Derivatives as Potent Inhibitors of Influenza Virus Neuraminidase. Bioorg Med Chem. 2006, 14, 8574-8581.
14. M. Zheng, K. Yu, H. Liu, X. Luo, K. Chen, W. Zhu, and H. Jiang. QSAR Analyses on Avian Influenza Virus Neuraminidase Inhibitors Using CoMFA, CoMSIA, and HQSAR. J Comput Aided Mol Des. 2006, 20, 549-566.
15. B. J. Smith, T. Huyton, R. P. Joosten, J. L. McKimm-Breschkin, J. G. Zhang, C. S. Luo, M. Z. Lou, N. E. Labrou, and T. P. J. Garrett. Structure of a Calcium-deficient Form of Influenza Virus Neuraminidase: Implications for Substrate Binding. Acta. Crystallogr. D. 2006, 62, 947-952.
16. C. Barillari, J. Taylor, R. Viner, and J. W. Essex. Classification of Water Molecules in Protein Binding Sites. J. Am. Chem. Soc. 2007, 129, 2577-2587.
17. A. K. Chong, M. S. Pegg, and M. von Itzstein. Influenza Virus Sialidase: Effect of Calcium on Steady-state Kinetic Parameters. Biochim. Biophys. Acta 1991, 1077, 65-71.
18. J. D. Dunitz. The Entropic Cost of Bound Water in Crystals and Biomolecules. Science 1994, 264, 670.
19. C. de Graaf, P. Pospisil, W. Pos, G. Folkers, and N. P. E. Vermeulen. Binding Mode Prediction of Cytochrome P450 and Thymidine Kinase Protein-ligand Complexes by Consideration of Water and Rescoring in Automated Docking. J. Med. Chem. 2005, 48, 2308-2318.
20. M. L. Verdonk, G. Chessari, J. C. Cole, M. J. Hartshorn, C. W. Murray, J. W. M. Nissink, R. D. Taylor, and R. Taylor. Modeling Water Molecules in Protein-ligand Docking Using GOLD. J. Med. Chem. 2005, 48, 6504-6515.
21. A. T. Garcia-Sosa and R. L. Mancera. The Effect of a Tightly Bound Water Molecule on Scaffold Diversity in the Computer-aided de Novo Ligand Design of CDK2 Inhibitors. J. Mol. Model. 2006, 12, 422-431.
22. B. J. Smith, P. M. Colman, M. Von Itzstein, B. Danylec, and J. N. Varghese. Analysis of Inhibitor Binding in Influenza Virus Neuraminidase. Protein Sci. 2001, 10, 689-696.
23. P. Bonnet and R. A. Bryce. Molecular Dynamics and Free Energy Analysis of Neuraminidase-ligand Interactions. Protein Sci. 2004, 13, 946-957.
24. R. L. Mancera. De Novo Ligand Design with Explicit Water Molecules: an Application to Bacterial Neuraminidase. J. Comput. Aided Mol. Des. 2002, 16, 479-499.
25. L. Birch, C. W. Murray, M. J. Hartshorn, I. J. Tickle, and M. L. Verdonk. Sensitivity of Molecular Docking to Induced Fit Effects in Influenza Virus Neuraminidase. J. Comput. Aided Mol. Des. 2002, 16, 855-869.
26. M. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, V. G. Zakrzewski, J. A. Montgomery Jr., R. E. Stratmann, J. C. Burant, S. Dapprich, J. M. Millam, A. D. Daniels, K. N. Kudin, M. C. Strain, O. Farkas, J. Tomasi, V. Barone, M. Cossi, R. Cammi, B. Mennucci, C. Pomelli, C. Adamo, S. Clifford, J. Ochterski, G. A. Petersson, P. Y. Ayala, Q. Cui, K. Morokuma, D. K. Malick, A. D. Rabuck, K. Raghavachari, J. B. Foresman, J. Cioslowski, J. V. Ortiz, A. G. Baboul, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. Gomperts, R. L. Martin, D. J. Fox, T. Keith, M. A. Al-Laham, C. Y. Peng, A. Nanayakkara, C. Gonzalez, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, J. L. Andres, C. Gonzalez, M. Head-Gordon, E. S. Replogle, and J. A. Pople. Gaussian 98, Revision A.9, Gaussian, Inc., Pittsburgh, PA, (1998).
27. G. Yang, X. W. Han, X. M. Liu, P. Y. Yang, Y. G. Zhou, and X. H. Bao. Study on Conformation Interconversion of 3-alkyl-4-acetyl-3,4-dihydro-2H- 1,4- benzo- xazines from Dynamic NMR Experiments and Ab Initio Density Functional Calculations. J. Phys. Chem. B 2005, 109, 18690-18698.
28. W. Humphrey, A. Dalke, and K. Schulten. VMD: Visual Molecular Dynamics. J. Mol. Graph. 1996, 14, 33-38.
29. W. Kabsch and C. Sander. Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-bonded and Geometrical Features. Biopolymers 1983, 22, 2577-2637.
30. R. C. Wade. 'Flu' and Structure-based Drug Design. Structure 1997, 5, 1139-1145.
31. G. T. Wang, Y. W. Chen, S. Wang, R. Gentles, T. Sowin, W. Kati, S. Muchmore, V. Giranda, K. Stewart, H. Sham, D. Kempf, and W. G. Laver. Design, Synthesis, and Structural Analysis of Influenza Neuraminidase Inhibitors Containing Pyrrolidine Cores. J. Med. Chem. 2001, 44, 1192-1201.
32. V. Stoll, K. D. Stewart, C. J. Maring, S. Muchmore, V. Giranda, Y. G. Gu, G. Wang, Y. W. Chen, M. H. Sun, C. Zhao, A. L. Kennedy, D. L. Madigan, Y. B. Xu, A. Saldivar, W. Kati, G. Laver, T. Sowin, H. L. Sham, J. Greer, and D. Kempf. Influenza Neuraminidase Inhibitors: Structure-based Design of a Novel Inhibitor Series. Biochemistry 2003, 42, 718-727.
33. P. Chand, Y. S. Babu, S. Bantia, N. Chu, L. B. Cole, P. L. Kotian, W. G. Laver, J. A. Montgomery, V. P. Pathak, S. L. Petty, D. P. Shrout, D. A. Walsh, and G. M. Walsh. Design and Synthesis of Benzoic Acid Derivatives as Influenza Neuraminidase Inhibitors Using Structure-based Drug Design. J. Med. Chem. 1997, 40, 4030-4052.
34. M. A. Williams, W. Lew, D. B. Mendel, C. Y. Tai, P. A. Escarpe, W. G. Laver, R. C. Stevens, and C. U. Kim. Structure-activity Relationships of Carbocyclic Influenza Neuraminidase Inhibitors. Bioorg. Med. Chem. Lett. 1997, 7, 1837-1842.
35. C. U. Kim, W. Lew, M. A. Williams, H. W. Wu, L. J. Zhang, X. W. Chen, P. A. Escarpe, D. B. Mendel, W. G. Laver, and R. C. Stevens. Structure-activity Relationship Studies of Novel Carbocyclic Influenza Neuraminidase Inhibitors. J. Med. Chem. 1998, 41, 2451-2460.
36. 3-aza Carbocyclic Influenza Neuraminidase Inhibitors: Synthesis and Inhibitory Activity. Bioorg. Med. Chem. Lett. 1998, 8, 3321-3324.
37. V. R. Atigadda, W. J. Brouillette, F. Duarte, S. M. Ali, Y. S. Babu, S. Bantia, P. Chand, N. M. Chu, J. A. Montgomery, D. A. Walsh, E. A. Sudbeck, J. Finley, M. Luo, G. M. Air, and G. W. Laver. Potent Inhibition of Influenza Sialidase by a Benzoic Acid Containing a 2-Pyrrolidinone Substituent. J. Med. Chem. 1999, 42, 2332-2343.
38. P. Chand, Y. S. Babu, S. Bantia, S. Rowland, A. Dehghani, P. L. Kotian, T. L. Hutchison, S. Ali, W. Brouillette, Y. El-Kattan, and T. H. Lin. Syntheses and Neuraminidase Inhibitory Activity of Multisubstituted Cyclopentane Amide Derivatives. J. Med. Chem. 2004, 47, 1919-1929.
39. C. J. Maring, V. S. Stoll, C. Zhao, M. H. Sun, A. C. Krueger, K. D. Stewart, D. L. Madigan, W. M. Kati, Y. B. Xu, R. J. Carrick, D. A. Montgomery, A. Kempf-Grote, K. C. Marsh, A. Molla, K. R. Steffy, H. L. Sham, W. G. Laver, Y. G. Gu, D. J. Kempf, and W. E. Kohlbrenner. Structure-based Characterization and Optimization of Novel Hydrophobic Binding Interactions in a Series of Pyrrolidine Influenza Neuraminidase Inhibitors. J. Med. Chem. 2005, 48, 3980-3990.
40. G. Yang, Z. W. Yang, X. M. Wu, and Y. G. Zu. A Novel Anti-influenza Drug: Molecular Docking of Trihydroxymethoxyflavone. Chin. Comput. Appl. Chem. 2008, 25, 409-414.
41. T. Takahashi, T. Suzuki, K. I. Hidari, D. Miyamoto, and Y. Suzuki. A Molecular Mechanism for the Low-pH Stability of Sialidase Activity of Influenza A Virus N2 Neuraminidases. FEBS. Lett. 2003, 543, 71-75.
42. K. M. Masukawa, P. A. Kollman, and I. D. Kuntz. Investigation of Neuraminidase-substrate Recognition Using Molecular Dynamics and Free Energy Calculations. J. Med. Chem. 2003, 46, 5628-5637.
43. V. R. Atigadda, W. J. Brouillette, F. Duarte, Y. S. Babu, S. Bantia, P. Chand, N. M. Chu, J. A. Montgomery, D. A. Walsh, E. Sudbeck, J. Finley, G. M. Air, M. Luo, and G. W. Laver. Hydrophobic Benzoic Acids as Inhibitors of Influenza Neuraminidase. Bioorg. Med. Chem. 1999, 7, 2487-2497.
44. N. Brooijmans and I. D. Kuntz. Molecular Recognition and Docking Algorithms. Annu. Rev. Biophys. Biomol. Struct. 2003, 32, 335-373.