Liver fluke β-tubulin isotype 2 binds albendazole and is thus a probable target of this drug

Parasitology Research

Volumn 107, Issue 5, 2010, Pages 1257-1264

  Chambers, Emma ^a,b   Ryan, Louise A ^a,c   Hoey, Elizabeth M ^a   Trudgett, Alan ^a   McFerran, Neil V ^a   Fairweather, Ian ^a   Timson, David J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b South Eastern Regional College   (United Kingdom)

^c Abbott Ireland Diagnostic Division   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ALBENDAZOLE; ANTHELMINTIC AGENT; HELMINTH PROTEIN; ISOPROTEIN; RECOMBINANT PROTEIN; TUBULIN;

ANIMAL; ARTICLE; BINDING SITE; BIOSYNTHESIS; CHEMICAL STRUCTURE; DRUG EFFECT; ESCHERICHIA COLI; FASCIOLA HEPATICA; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

ALBENDAZOLE; ANIMALS; ANTHELMINTICS; BINDING SITES; ESCHERICHIA COLI; FASCIOLA HEPATICA; HELMINTH PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TUBULIN;

EID: 79952111449     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-010-1997-5     Document Type: Article

References (46)

1. Alvarez L, Moreno G, Moreno L, Ceballos L, Shaw L, Fairweather I, Lanusse C (2009) Comparative assessment of albendazole and triclabendazole ovicidal activity on Fasciola hepatica eggs. Vet Parasitol 164:211-216
2. Arguello-Garcia R, Cruz-Soto M, Romero-Montoya L, Ortega-Pierres G (2009) In vitro resistance to 5-nitroimidazoles and benzimidazoles in Giardia duodenalis: variability and variation in gene expression. Infect Genet Evol 9:1057-1064
3. Boray JC (1994) Diseases of domestic animals caused by flukes. F.A. O, Rome, pp 1-32
4. Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy M, McConville M, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Alvarez L, Solana H, Virkel G, Brophy PM (2007) Understanding triclabendazole resistance. Exp Mol Pathol 82:104-109 (Pubitemid 46505133)
5. Buchanan JF, Fairweather I, Brennan GP, Trudgett A, Hoey EM (2003) Fasciola hepatica: surface and internal tegumental changes induced by treatment in vitro with the sulphoxide metabolite of albendazole ('Valbazen'). Parasitology 126:41-153
6. Chambers E, Hoey EM, Trudgett A, Fairweather I, Timson DJ (2010) Binding of serum albumin to the anthelmintic drugs albendazole, triclabendazole and their sulphoxides. Vet Parasitol 171(1-2):172-175
7. Chu SW, Badar S, Morris DL, Pourgholami MH (2009) Potent inhibition of tubulin polymerisation and proliferation of paclitaxel-resistant 1A9PTX22 human ovarian cancer cells by albendazole. Anticancer Res 29:3791-3796
8. Cline GW, Hanna SB (1987) The aminolysis of N-hydroxysuccinimide esters. A structure-reactivity study. J Am Chem Soc 109:3087-3091
9. Cruz MC, Edlind T (1997) β-Tubulin genes and the basis for benzimidazole sensitivity of the opportunistic fungus Cryptococcus neoformans. Microbiology 143:2003-2008 (Pubitemid 27290292)
10. Elard L, Comes AM, Humbert JF (1996) Sequences of β-tubulincDNA from benzimidazole-susceptible and -resistant strains of Teladorsagia circumcincta, a nematode parasite of small ruminants. Mol Biochem Parasitol 79:249-253 (Pubitemid 26241898)
11. Fairweather I (2005) Triclabendazole: new skills to unravel an old(ish) enigma. J Helminthol 79:227-234
12. Fairweather I (2009) Triclabendazole progress report, 2005-2009: an advancement of learning? J Helminthol 83:139-150
13. Fetterer RH (1986) The effect of albendazole and triclabendazole on colchicine binding in the liver fluke Fasciola hepatica. J Vet Pharmacol Ther 9:49-54
14. Ghisi M, Kaminsky R, Maser P (2007) Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet Parasitol 144:313-320
15. Halferty L, Brennan GP, Trudgett A, Hoey L, Fairweather I (2009) Relative activity of triclabendazole metabolites against the liver fluke, Fasciola hepatica. Vet Parasitol 159:126-138
16. Henriquez FL, Ingram PR, Muench SP, Rice DW, Roberts CW (2008) Molecular basis for resistance of Acanthamoeba tubulins to all major classes of antitubulin compounds. Antimicrob Agents Chemother 52:1133-1135 (Pubitemid 351358398)
17. Hoti SL, Subramaniyan K, Das PK (2003) Detection of codon for amino acid 200 in isotype 1 β-tubulin gene of Wuchereria bancrofti isolates, implicated in resistance to benzimidazoles in other nematodes. Acta Trop 88:77-81 (Pubitemid 37013339)
18. Jimenez-Gonzalez A, De Armas-Serra C, Criado-Fornelio A, Casado- Escribano N, Rodriguez-Caabeiro F, Diez JC (1991) Preliminary characterization and interaction of tubulin from Trichinella spiralis larvae with benzimidazole derivatives. Vet Parasitol 39:89-99
19. Kenyon F, Sargison ND, Skuce PJ, Jackson F (2009) Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Vet Parasitol 163:293-297
20. Kwa MS, Veenstra JG, Roos MH (1994) Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1. Mol Biochem Parasitol63:299-303 (Pubitemid 24073839)
21. Lacey E, Prichard RK (1986) Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus. Mol Biochem Parasitol 19:171-181 (Pubitemid 16076530)
22. Lowe J, Li H, Downing KH, Nogales E (2001) Refined structure of αβ-tubulin at 3.5 Å resolution. J Mol Biol 313:1045-1057 (Pubitemid 33081900)
23. Lubega GW, Prichard RK (1990) Specific interaction of benzimidazole anthelmintics with tubulin: high-affinity binding and benzimidazole resistance in Haemonchus contortus. Mol Biochem Parasitol 38:221-232 (Pubitemid 20023136)
24. Lubega GW, Prichard RK (1991) Interaction of benzimidazole anthelmintics with Haemonchus contortus tubulin: binding affinity and anthelmintic efficacy. Exp Parasitol 73:203-213
25. MacDonald LM, Armson A, Thompson AR, Reynoldson JA (2004) Characterisation of benzimidazole binding with recombinant tubulin from Giardia duodenalis, Encephalitozoon intestinalis, and Cryptosporidium parvum. Mol Biochem Parasitol 138:89-96 (Pubitemid 39410530)
26. Marshak DR, Watterson DM, Van Eldik LJ (1981) Calcium-dependent interaction of S100b, troponin C, and calmodulin with an immobilized phenothiazine. Proc Natl Acad Sci USA 78:6793-6797 (Pubitemid 12216847)
27. Mas-Coma S, Valero MA, Bargues MD (2009a) Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69:41-146
28. Mas-Coma S, Valero MA, Bargues MD (2009b) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol 163:264-280
29. McConville M, Brennan GP, McCoy M, Castillo R, Hernandez-Campos A, Ibarra F, Fairweather I (2006) Adult triclabendazole-resistant Fasciola hepatica: surface and subsurface tegumental responses to in vitro treatment with the sulphoxide metabolite of the experimental fasciolicide compound alpha. Parasitology 133:195-208 (Pubitemid 44099907)
30. Moll L, Gaasenbeek CP, Vellema P, Borgsteede FH (2000) Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in The Netherlands. Vet Parasitol 91:153-158 (Pubitemid 30411964)
31. Nogales E, Wolf SG, Downing KH (1998) Structure of the αβ tubulin dimer by electron crystallography. Nature 391:199-203 (Pubitemid 28092482)
32. Oxberry ME, Geary TG, Winterrowd CA, Prichard RK (2001) Individual expression of recombinant α- and β-tubulin from Haemonchus contortus: polymerization and drug effects. Protein Expr Purif 21:30-39 (Pubitemid 32614493)
33. Pathmanathan S, Elliott SF, McSwiggen S, Greer B, Harriott P, Irvine GB, Timson DJ (2008) IQ motif selectivity in human IQGAP1: binding of myosin essential light chain and S100B. Mol Cell Biochem 318:43-51
34. Prichard R (2001) Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends Parasitol 17:445-453
35. Robinson MW, Dalton JP (2009) Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Phil Trans R Soc B 364:2763-2776
36. Robinson MW, Hoey EM, Fairweather I, Dalton JP, McGonigle S, Trudgett A (2001) Characterisation of a β-tubulin gene from theliver fluke, Fasciola hepatica. Int J Parasitol 31:1264-1268 (Pubitemid 32762997)
37. Robinson MW, Trudgett A, Hoey EM, Fairweather I (2002) Triclabendazole-resistant Fasciola hepatica: β-tubulin and responseto in vitro treatment with triclabendazole. Parasitology 124:325-338 (Pubitemid 34250745)
38. Robinson MW, Trudgett A, Hoey EM, Fairweather I (2003) The effect of the microtubule inhibitor tubulozole-C on the tegument of triclabendazole- susceptible and triclabendazole-resistant Fasciola hepatica. Parasitol Res 91:117-129 (Pubitemid 37204523)
39. Robinson MW, McFerran N, Trudgett A, Hoey L, Fairweather I (2004) A possible model of benzimidazole binding to β-tubulindisclosed by invoking an inter-domain movement. J Mol Graph Model 23:275-284 (Pubitemid 39463106)
40. Ryan LA, Hoey E, Trudgett A, Fairweather I, Fuchs M, Robinson MW, Chambers E, Timson DJ, Ryan E, Feltwell T, Ivens A, Bentley G, Johnston D (2008) Fasciola hepatica expresses multiple α- and β-tubulin isotypes. Mol Biochem Parasitol 159:73-78 (Pubitemid 351469922)
41. Schwab AE, Boakye DA, Kyelem D, Prichard RK (2005) Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. Am J Trop Med Hyg 73:234-238 (Pubitemid 41278690)
42. Schwenkenbecher JM, Kaplan RM (2009) Real-time PCR assays for monitoring benzimidazole resistance-associated mutations in Ancylostoma caninum. Exp Parasitol 122:6-10
43. Sellick CA, Reece RJ (2003) Modulation of transcription factor function by an amino acid: activation of Put3p by proline. EMBO J 22:5147-5153 (Pubitemid 37222034)
44. Solana HD, Teruel MT, Najle R, Lanusse CE, Rodriguez JA (1998) The anthelmintic albendazole affects in vivo the dynamics and the detyrosination-tyrosination cycle of rat brain microtubules. Acta Physiol Pharmacol Ther Latinoam 48:199-205 (Pubitemid 29042317)
45. Thomas I, Coles GC, Duffus K (2000) Triclabendazole-resistant Fasciola hepatica in southwest Wales. Vet Rec 146:200 (Pubitemid 30102785)
46. Upcroft J, Mitchell R, Chen N, Upcroft P (1996) Albendazole resistance in Giardia is correlated with cytoskeletal changes but not with a mutation at amino acid 200 in β-tubulin. Microb DrugResist 2:303-308