Towards the identification of the binding site of benzimidazoles to β-tubulin of Trichinella spiralis: Insights from computational and experimental data

Journal of Molecular Graphics and Modelling

Volumn 41, Issue , 2013, Pages 12-19

  Aguayo Ortiz, Rodrigo ^a   Méndez Lucio, Oscar ^a   Medina Franco, José L ^a   Castillo, Rafael ^a   Yépez Mulia, Lilián ^b   Hernández Luis, Francisco ^a   Hernández Campos, Alicia ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

Tubulin; Benzimidazole 2 carbamate derivatives; Docking; Homology modeling; Molecular dynamics; Trichinella spiralis

Indexed keywords

AMINO ACID SEQUENCE; COMPETITIVE INHIBITION; CRYSTALLOGRAPHIC STRUCTURE; HOMOLOGY MODELING; MECHANISM OF ACTION; MICROTUBULE POLYMERIZATION; MOLECULAR DYNAMICS CALCULATION; TRICHINELLA SPIRALIS;

AMINO ACIDS; DOCKING; HYDROGEN BONDS;

MOLECULAR DYNAMICS;

ALBENDAZOLE; ALBENDAZOLE SULFOXIDE; BENZIMIDAZOLE DERIVATIVE; BETA TUBULIN; CARBENDAZIM; COLCHICINE; CYSTINE; FENBENDAZOLE; GLUTAMIC ACID; GLYCINE; LUXABENDAZOLE; MEBENDAZOLE; NOCODAZOLE; OXFENDAZOLE; OXIBENDAZOLE; PARBENDAZOLE; THREONINE;

ARTICLE; BINDING SITE; CHEMICAL BINDING; COMPUTER ANALYSIS; DRUG RESISTANCE; DRUG STRUCTURE; GENE MUTATION; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; TRICHINELLA SPIRALIS;

AMINO ACID SEQUENCE; ANIMALS; ANTHELMINTICS; BENZIMIDAZOLES; BINDING SITES; CARBAMATES; COLCHICINE; DRUG RESISTANCE; HELMINTH PROTEINS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; THERMODYNAMICS; TRICHINELLA SPIRALIS; TUBULIN;

TRICHINELLA SPIRALIS;

EID: 84875538937     PISSN: 10933263     EISSN: 18734243     Source Type: Journal    
DOI: 10.1016/j.jmgm.2013.01.007     Document Type: Article

References (52)

1. P.J. Hotez Neglected infections of poverty in the United States of America PLOS Neglected Tropical Diseases 2 2008 e256
2. K.H. Downing Structural basis for the interaction of tubulin with proteins and drugs that affect microtubule dynamics Annual Review of Cell and Developmental Biology 16 2000 89 111
3. B.J. Fennell, J.A. Naughton, J. Barlow, G. Brennan, and I. Fairweather Microtubules as antiparasitic drug targets Expert Opinion 3 2008 501 518
4. L. Mottier, and C.E. Lanusse Bases moleculares de la resistencia a fármacos antihelmínticos Revista de Medicina Veterinaria 82 2001 74 85
5. S.K. Katiyar, V.R. Gordon, G.L. McLaughlin, and T.D. Edlind Antiprotozoal activities of benzimidazoles and correlations with β-tubulin sequence Antimicrobial Agents and Chemotherapy 38 1994 2086 2090
6. S. Sharma, and N. Anand Approaches to Design and Synthesis of Antiparasitic Drugs vol. 25 1997 Elsevier Amsterdam Chapter 8
7. G.W. Lubega, and R.K. Prichard Specific interaction of benzimidazoles anthelmintics with tubulin: high-affinity binding and benzimidazoles resistance in Haemonchus contortus Molecular and Biochemical Parasitology 38 1990 221 232
8. A. Jiménez-González, C. De Armas-Serra, A. Criado-Fornelio, N. Casado Escribano, and F. Rodríguez-Caabeiro Preliminary characterization and interaction of tubulin from Trichinella spiralis larvae with benzimidazole derivatives Veterinary Parasitology 39 1991 89 99
9. M. Borgers, S. De Nollin, M. De Brabander, and D. Thienpont Influence of the anthelmintic mebendazole on microtubules and intracellular organelle movement in nematode intestinal cells American Journal of Veterinary Research 36 1975 1153 1166
10. E. Lacey, K.L. Snowdon, G.K. Eagleson, and E.F. Smith Further investigations of the primary mechanism of benzimidazole resistance in Haemonchus contortus International Journal for Parasitology 17 1987 1421 1429
11. E. Lacey, and J.H. Gill Biochemistry of benzimidazole resistance Acta Tropica 56 1994 245 262
12. B. Wallner, and A. Elofsson All are not equal: a benchmark of different homology modeling programs Protein Science 14 2005 1315 1327
13. C.N. Cavasotto Homology models in docking and high-throughput docking Current Topics in Medicinal Chemistry 11 2011 1528 1534
14. R.N. Beech, P. Skuce, D.J. Bartley, R.J. Martin, and R.K. Prichard Anthelmintic resistance: markers for resistance or susceptibility? Parasitology 138 2010 160 174
15. M. Ghisi, R. Kaminsky, and P. Mäser Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes Veterinary Parasitology 144 2007 313 320
16. L. Rufener, R. Kaminsky, and P. Mäser In vitro selection of Haemonchus contortus for benzimidazole resistance reveals a mutation at amino acid 198 of β-tubulin Molecular and Biochemical Parasitology 168 2009 120 122
17. M.S.G. Kwa, J.G. Veenstra, and M.H. Roos Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1 Molecular and Biochemical Parasitology 63 1994 299 303
18. P. Shayan, A. Eslami, and H. Borji Innovative restriction site created PCR-RFLP for detection of benzimidazole resistance in Teladorsagia circumcincta Parasitology Research 100 2006 1063 1068
19. A. Diawara, L.J. Drake, R.R. Suswillo, J. Kihara, and D.A.P. Bundy Assays to detect β-tubulin codon 200 polymorphism in Trichuris trichiura and Ascaris lumbricoides PLOS Neglected Tropical Diseases 3 2009 e397
20. A.E. Schwab, D.A. Boakye, D. Kyelem, and R.K. Prichard Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment The American Journal of Tropical Medicine and Hygiene 73 2005 234 238
21. M.W. Robinson, N. McFerran, A. Trudgett, L. Hoey, and I. Fairweather A possible model of benzimidazole binding to β-tubulin disclosed by invoking an inter-domain movement Journal of Molecular Graphics and Modelling 23 2004 275 284
22. F.L. Henriquez, P.R. Ingram, S.P. Muench, D.W. Rice, and C.W. Roberts Molecular basis for resistance of Acanthamoeba tubulins to all major classes of antitubulin compounds Antimicrobial Agents and Chemotherapy 52 2007 1133 1135
23. E. Chambers, L.A. Ryan, E.M. Hoey, A. Trudgett, and N.V. McFerran Liver fluke β-tubulin isotype 2 binds albendazole and is thus a probable target of this drug Parasitology Research 107 2010 1257 1264
24. O.P. Sharma, A. Pan, S.L. Hoti, A. Jadhav, and M. Kannan Modeling docking, simulation, and inhibitory activity of the benzimidazole analogue against β-tubulin protein from Brugia malayi for treating lymphatic filariasis Medicinal Chemistry Research 21 2011 2415 2427
25. P.A. Friedman, and E.G. Platzer Interaction of anthelmintic benzimidazole derivatives with bovine brain tubulin Biochimica et Biophysica Acta 544 1978 605 614
26. J.P. Laclette, G. Guerra, and C. Zetina Inhibition of tubulin polymerization by mebendazole Biochemical and Biophysical Research Communications 92 1980 417 423
27. 3H] benzimidazole carbamatos to mammalian brain tubulin and the mechanism of selective toxicity of the benzimidazole anthelmintics Biochemical Pharmacology 43 1992 1095 1100
28. S.K. Tahir, P. Kovar, S.H. Rosenberg, and S.C. Ng Rapid colchicine competition-binding scintillation proximity assay using biotin-labeled tubulin Biotechniques 29 2000 156 160
29. T.L. Nguyen, C. McGrath, A.R. Hermone, J.C. Burnett, and D.W. Zaharevitz A common pharmacophore for a diverse set of colchicine site inhibitors using a structure-based approach Journal of Medicinal Chemistry 48 2005 6107 6116
30. M. Mitreva, D.P. Jasmer, D.S. Zarlenga, Z. Wang, and S. Abubucker The draft genome of the parasitic nematode Trichinella spiralis Nature Genetics 43 2011 228 235
31. A. Roy, A. Kucukural, and Y. Zhang I-TASSER: a unified platform for automated protein structure and function prediction Nature Protocols 5 2010 725 738
32. P. Barbier, A. Dorleans, F. Devred, L. Sanz, and D. Allegro Stathmin and interfacial microtubule inhibitors recognize a naturally curved conformation of tubulin dimers Journal of Biological Chemistry 285 2010 31672 31681
33. A. Fiser, R.K. Do, and A. Sali Modeling of loops in protein structures Protein Science 9 2000 1753 1773
34. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures Journal of Applied Crystallography 26 1993 283 291
35. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, and A.E. Mark GROMACS: fast, flexible, and free Journal of Computational Chemistry 26 2005 1701 1718
36. M.F. Sanner Python: a programming language for software integration and development Journal of Molecular Graphics and Modelling 17 1999 57 61
37. A.W. Schüttelkopf, D.M.F., and V.A.N. Aalten PRODRG-a tool for highthroughput crystallography of protein-ligand complexes Acta Crystallographica 60 2004 1355 1363
38. W.F. van Gunsteren, S.R., Billeter, A.A., Eising, P.H. Hünenberger, P. Krüger, et al. Biomolecular Simulation: The GROMOS96 Manual and User Guide, Vdf Hochschulverlag AG an der ETH Zürich, Zürich, Switzerland, 1996, pp. 1-1042.
39. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems Journal of Chemical Physics 98 1993 10089
40. J. Aqvist, C. Medina, and J.E. Samuelsson A new method for predicting binding affinity in computer-aided drug design Protein Engineering 7 1994 385 391
41. A. Punkvang, P. Saparpakorn, S. Hannongbua, P. Wolschann, and A. Beyer Investigating the structural basis of arylamides to improve potency against M. tuberculosis strain through molecular dynamics simulations European Journal of Medical Chemistry 45 2010 5585 5593
42. A. Silvestre, and J. Cabaret Mutation in position 167 of isotype 1 β-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Molecular and Biochemical Parasitology 120 2002 297 300
43. P. Benkert, M. Kunzli, and T. Schwede QMEAN server for protein model quality estimation Nucleic Acids Research 37 2009 W4 W510
44. J. Wang, B. Czech, A. Crunk, A. Wallace, and M. Mitreva Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles Genome Research 21 2011 1462 1477
45. A.B. Bennett, G.C. Barker, and D.A.P. Bundy A beta-tubulin gene from Trichuris trichiura Molecular and Biochemical Parasitology 103 1999 111 116
46. C. Laurence, and M. Berthelot Observations on the strength of hydrogen bonding Perspectives in Drug Discovery and Design 18 2000 39 60
47. L.I. Álvarez, F.A. Imperiale, S.F. Sánchez, G.A. Murno, and C.E. Lanusse Uptake of albendazole and albendazole sulphoxide by Haemonchus contortus and Fasciola hepatica in sheep Veterinary Parasitology 94 2000 75 89
48. B.P.S. Capece, G.L. Virkel, and C.E. Lanusse Enantiomeric behaviour of albendazole and fenbendazole sulfoxides in domestic animals: pharmacological implications The Veterinary Journal 181 2009 241 250
49. E. Nogales Structure insights into microtubule function Annual Review of Biochemistry 69 2000 277 302
50. A. Dorléans, B. Gigant, R.B.G. Ravelli, P. Mailliet, and V. Mikol Variations in the colchicine-binding domain provide insight into the structural switch of tubulin Proceedings of the National Academy of Sciences of the United States of America 106 2009 13775 13779
51. A. Nawrotek, M. Knossow, and B. Gigant The determinants that govern microtubule assembly from the atomic structure of GTP-tubulin Journal of Molecular Biology 412 2011 35 42
52. W.L. DeLano The PyMOL Molecular Graphics System 2007 DeLano Scientific LLC Palo Alto, CA