Anthelmintic resistance: Markers for resistance, or susceptibility?

Parasitology

Volumn 138, Issue 2, 2011, Pages 160-174

  Beech, R N ^a   Skuce, P ^b   Bartley, D J ^b   Martin, R J ^c   Prichard, R K ^a   Gilleard, J S ^d  

^a MCGILL UNIVERSITY   (Canada)

^b MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^c IOWA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

anthelmintic resistance; benzimidazole; beta tubulin; levamisole; ligand gated ion channel; macrocyclic lactone; monepantel; P glycoprotein

Indexed keywords

BENZIMIDAZOLE DERIVATIVE; BIOLOGICAL MARKER; GLYCOPROTEIN P; IVERMECTIN; LEVAMISOLE; MONEPANTEL; MOXIDECTIN;

AMINO ACID SUBSTITUTION; ANTIHELMINTIC RESISTANCE; DRUG BINDING; DRUG MECHANISM; DRUG RESISTANCE; DRUG SENSITIVITY; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; NEMATODE; NONHUMAN; PARASITE ISOLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID SUBSTITUTION; ANIMALS; ANTHELMINTICS; BENZIMIDAZOLES; BIOLOGICAL MARKERS; CHOLINERGIC ANTAGONISTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; HELMINTHS; LIGAND-GATED ION CHANNELS; MACROCYCLIC COMPOUNDS; MALE; P-GLYCOPROTEIN; PARASITIC SENSITIVITY TESTS; TUBULIN;

NEMATODA;

EID: 79952986488     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182010001198     Document Type: Review

References (93)

1. Absalom, N. L., Lewis, T. M. and Schofield, P. R. (2004). Mechanisms of channel gating of the ligand-gated ion channel superfamily inferred from protein structure. Experimental Physiology 89, 145-153. (Pubitemid 38379939)
2. Ardleli, B. F. and Prichard, R. K. (2004). Identification of variant ABC-transporter genes among Onchocerca volvulus collected from ivermectin-treated and untreated patients in Ghana, West Africa. Annals of Tropical Medicine and Parasitology 98, 371-384. (Pubitemid 38903481)
3. Ardleli, B. F., Stitt, L. E., Tompkins, J. B. and Prichard, R. K. (2009). A comparison of the effects of ivermectin and moxidectin on the nematode Caenorhabditis elegans. Veterinary Parasitology 165, 96-108.
4. Ballivet, M., Alliod, C., Bertrand, S. and Bertrand, D. (1996). Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. Journal of Molecular Biology 258, 261-269. (Pubitemid 26131730)
5. Beech, R. N., Prichard, R. K. and Scott, M. E. (1994). Genetic variability of the beta-tubulin genes in benzimidazole-susceptible and -resistant strains of Haemonchus contortus. Genetics 138, 103-110.
6. Beech, R. N. and Silvestre, A. (2010). Mutations associated with anthelmintic drug resistance. Anti-Infective Agents in Medicinal Chemistry 9, 105-112.
7. Beech, R. N., Wolstenholme, A. J., Neveu, C. and Dent, J. A. (2010). Nematode parasite genes, what's in a name? Trends in Parasitology 26, 334-340.
8. Berriman, M. (2009a). The Haemonchus contortus sequencing project http://www.sanger.ac.uk/Projects/ H-contortus/
9. Berriman, M. (2009b). The Teladorsagia circumcincta sequencing project http://www.sanger.ac.uk/Projects/ H-contortus/
10. Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature, London 460, 352-358.
11. Bhargava, A. and Fuentes, F. F. (2010). Mutational dynamics of microsatellites. Molecular Biotechnology 44, 250-266.
12. Blackhall, W. J., Prichard, R. K. and Beech, R. N. (2008). P-glycoprotein selection in strains of Haemonchus contortus resistant to benzimidazoles. Veterinary Parasitology 152, 101-107.
13. Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 71-75. (Pubitemid 28150590)
14. Boulin, T., Gielen, M., Richmond, J. E., Williams, D. C., Paoletti, P. and Bessereau, J. L. (2008). Eight genes are required for functional reconstitution of the Caenorhabditis elegans levamisole-sensitive acetylcholine receptor. Proceedings of the National Academy of Sciences, USA 105, 18590-18595.
15. Bourguinat, C., Ardelli, B. F., Pion, S. D., Kamgno, J., Gardon, J., Duke, B. O., Boussinesq, M. and Prichard, R. K. (2008). P-glycoprotein-like protein, a possible genetic marker for ivermectin resistance selection in Onchocerca volvulus. Molecular and Biochemical Parasitology 158, 101-111. (Pubitemid 351255520)
16. Cabaret, J. (2008). Pro and cons of targeted selective treatment against digestive-tract strongyles of ruminants. Parasite 15, 506-509.
17. Chen, C., Zhao, W., Lu, Y., Wang, J., Chen, Y., Li, H. and Zhou, M. (2009). High-throughput detection of highly benzimidazole-resistant allele E198A with mismatch primers in allele-specific real-time polymerase chain reaction. Pest Management Science 65, 413-419.
18. Conder, G. A., Jen, L.W., Marbury, K. S., Johnson, S. S., Guimond, P. M., Thomas, E. M. and Lee, B. L. (1990). A novel anthelmintic model utilizing jirds, Meriones unguiculatus, infected with Haemonchus contortus. Journal of Parasitology 76, 168-170. (Pubitemid 20156031)
19. Conder, G. A., Johnson, S. S., Guimond, P. M., Cox, D. L. and Lee, B. L. (1991a). Concurrent infections with the ruminant nematodes Haemonchus contortus and Trichostrongylus colubriformis in jirds, Meriones unguiculatus, and use of this model for anthelmintic studies. Journal of Parasitology 77, 621-623.
20. Conder, G. A., Johnson, S. S., Guimond, P. M., Geary, T. G., Lee, B. L., Winterrowd, C. A., Lee, B. H. and DiRoma, P. J. (1991b). Utility of a Haemonchus contortus/jird (Meriones unguiculatus) model for studying resistance to levamisole. Journal of Parasitology 77, 83-86.
21. Crowe, M. L. (2005). SeqDoC: Rapid SNP and mutation detection by direct comparison of DNA sequence chromatograms. BMC Bioinformatics 6, 133.
22. Cully, D. F. and Paress, P. S. (1991). Solubilization and characterization of a high affinity ivermectin binding site from Caenorhabditis elegans. Molecular Pharmacology 40, 326-332.
23. Cvilink, V., Lamka, J. and Skalova, L. (2009). Xenobiotic metabolizing enzymes and metabolism of anthelminthics in helminths. Drug Metabolism Reviews 41, 8-26.
24. de Lourdes Mottier, M. and Prichard, R. K. (2008). Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on Haemonchus contortus. Pharmacogenetics and Genomics 18, 129-140.
25. Dent, J. A., Smith, M. M., Vassilatis, D. K. and Avery, L. (2000). The genetics of ivermectin resistance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 97, 2674-2679. (Pubitemid 30159230)
26. Diawara, A., Drake, L. J., Suswillo, R. R., Kihara, J., Bundy, D. A., Scott, M. E., Halpenny, C., Stothard, J. R. and Prichard, R. K. (2009). Assays to detect beta-tubulin codon 200 polymorphism in Trichuris trichiura and Ascaris lumbricoides. PLoS Neglected Tropical Diseases 3, e397.
27. Driscoll, M., Dean, E., Reilly, E., Bergholz, E. and Chalfie, M. (1989). Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity. Journal of Cell Biology 109, 2993-3003. (Pubitemid 20011924)
28. Drudge, J. H., Szanto, J.,Wyant, Z. N. and Elam, G.W. (1964). Field studies on parasite control of sheep: Comparison of thiabendazole, ruelene and phenothiazine. American Journal of Veterinary Research 25, 1512-1518.
29. Fauvin, A., Charvet, C., Issouf, M., Cortet, J., Cabaret, J. and Neveu, C. (2010). cDNA-AFLP analysis in levamisole-resistant Haemonchus contortus reveals alternative splicing in a nicotinic acetylcholine receptor subunit. Molecular and Biochemical Parasitology 170, 105-107.
30. Feng, X. P., Hayashi, J., Beech, R. N. and Prichard, R. K. (2002). Study of the nematode putative GABA type-A receptor subunits: Evidence for modulation by ivermectin. Journal of Neurochemistry 83, 870-878. (Pubitemid 35316037)
31. Forrester, S. G., Prichard, R. K. and Beech, R. N. (2002).A glutamate-gated chloride channel subunit from Haemonchus contortus: Expression in a mammalian cell line, ligand binding, and modulation of anthelmintic binding by glutamate. Biochemical Pharmacology 63, 1061-1068. (Pubitemid 34267021)
32. Galazzo, D. (2004). A comparison of laboratory and field resistance to macrocyclic lactones in Haemonchus contortus. M.Sc. thesis. McGill University, Montreal, Canada.
33. Garg, R. and Yadav, C. L. (2008). Genotyping of benzimidazole susceptible and resistant alleles in different populations of Haemonchus contortus from Himalayan and sub-Himalayan regions of North-West India. Tropical Animal Health and Production 41, 1127-1131.
34. Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M.W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B.W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G.,Williams, D. J., Zhang, Y.,Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756-1760. (Pubitemid 47461841)
35. Ghisi, M., Kaminsky, R. and Maser, P. (2007). Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Veterinary Parasitology 144, 313-320.
36. Gilleard, J. S. and Beech, R. N. (2007). Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 1133-1147. (Pubitemid 47026659)
37. Grillo, V., Jackson, F., Cabaret, J. and Gilleard, J. S. (2007). Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology 37, 435-447. (Pubitemid 46231225)
38. Harhay, M. O., Horton, J. and Olliaro, P. L. (2010). Epidemiology and control of human gastrointestinal parasites in children. Expert Review of Anti Infective Therapy 8, 219-234.
39. Hodgkinson, J. E., Clark, H. J., Kaplan, R. M., Lake, S. L. and Matthews, J. B. (2008). The role of polymorphisms at beta tubulin isotype 1 codons 167 and 200 in benzimidazole resistance in cyathostomins. International Journal for Parasitology 38, 1149-1160.
40. Hoglund, J., Gustafsson, K., Ljungstrom, B. L., Engstrom, A., Donnan, A. and Skuce, P. (2009). Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the beta-tubulin gene. Veterinary Parasitology 161, 60-68.
41. Jablonka, E. and Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Quarterly Reviews in Biology 84, 131-176.
42. James, C. E. and Davey, M.W. (2009). Increased expression of ABC transport proteins is associated with ivermectin resistance in the model nematode Caenorhabditis elegans. International Journal for Parasitology 39, 213-220.
43. James, C. E., Hudson, A. L. and Davey, M.W. (2009). Drug resistance mechanisms in helminths: Is it survival of the fittest? Trends in Parasitology 25, 328-335.
44. Jones, A. K., Davis, P., Hodgkin, J. and Sattelle, D. B. (2007). The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: An update on nomenclature. Invertebrate Neuroscience 7, 129-131. (Pubitemid 46855267)
45. Kaminsky, R., Ducray, P., Jung, M., Clover, R., Rufener, L., Bouvier, J., Weber, S. S., Wenger, A., Wieland-Berghausen, S., Goebel, T., Gauvry, N., Pautrat, F., Skripsky, T., Froelich, O., Komoin- Oka, C., Westlund, B., Sluder, A. and Maser, P. (2008). A new class of anthelmintics effective against drug-resistant nematodes. Nature, London 452, 176-180. (Pubitemid 351380246)
46. Kenyon, F., Greer, A.W., Coles, G. C., Cringoli, G., Papadopoulos, E., Cabaret, J., Berrag, B., Varady, M., Van Wyk, J. A., Thomas, E., Vercruysse, J. and Jackson, F. (2009). The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Veterinary Parasitology 164, 3-11.
47. Kopp, S. R., Coleman, G. T., Traub, R. J., McCarthy, J. S. and Kotze, A. C. (2009). Acetylcholine receptor subunit genes from Ancylostoma caninum: Altered transcription patterns associated with pyrantel resistance. International Journal for Parasitology 39, 435-441.
48. Kotze, A. C., Dobson, R. J., Tyrrell, K. L. and Stein, P. A. (2002). High-level ivermectin resistance in a field isolate of Haemonchus contortus associated with a low level of resistance in the larval stage: Implications for resistance detection. Veterinary Parasitology 108, 255-263. (Pubitemid 35247783)
49. Kotze, A. C., Le Jambre, L. F. and O'Grady, J. (2006). A modified larval migration assay for detection of resistance to macrocyclic lactones in Haemonchus contortus, and drug screening with Trichostrongylidae parasites. Veterinary Parasitology 137, 294-305.
50. Krause, R. M., Buisson, B., Bertrand, S., Corringer, P. J., Galzi, J. L., Changeux, J. P. and Bertrand, D. (1998). Ivermectin: A positive allosteric effector of the alpha7 neuronal nicotinic acetylcholine receptor. Molecular Pharmacology 53, 283-294. (Pubitemid 28099739)
51. Kwa, M. S. G., Jetty, V. S. and Roos, M. H. (1994). 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, 299-303. (Pubitemid 24073839)
52. Le Jambre, L. F. (1993). Ivermectin-resistant Haemonchus contortus in Australia. Australian Veterinary Journal 70, 357.
53. Liu, F., Zhou, Y., Wang, Z. Q., Lu, G., Zheng, H., Brindley, P. J., McManus, D. P., Blair, D., Zhang, Q. H., Zhong, Y., Wang, S., Han, Z. G. and Chen, Z. (2009). The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature, London 460, 345-351.
54. Martin, R. J. (1996). An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutamate-gated chloride channel sensitive to the avermectin analogue, milbemycin D. Parasitology 112, 247-252. (Pubitemid 26069951)
55. Martin, R. J., Clark, C. L., Trailovic, S. M. and Robertson, A. P. (2004). Oxantel is an N-type (methyridine and nicotine) agonist not an L-type (levamisole and pyrantel) agonist: Classification of cholinergic anthelmintics in Ascaris. International Journal for Parasitology 34, 1083-1090. (Pubitemid 39093808)
56. Martin, R. J. and Pennington, A. J. (1989). A patch-clamp study of effects of dihydroavermectin on Ascaris muscle. British Journal of Pharmacolology 98, 747-756. (Pubitemid 19269797)
57. McCavera, S., Rogers, A. T., Yates, D. M.,Woods, D. J. and Wolstenholme, A. J. (2009). An ivermectin-sensitive glutamate-gated chloride channel from the parasitic nematode Haemonchus contortus. Molecular Pharmacology 75, 1347-1355.
58. McCavera, S., Walsh, T. K. and Wolstenholme, A. J. (2007). Nematode ligand-gated chloride channels: An appraisal of their involvement in macrocyclic lactone resistance and prospects for developing molecular markers. Parasitology 134, 1111-1121. (Pubitemid 47026657)
59. Merino, G., Real, R., Baro, M. F., Gonzalez- Lobato, L., Prieto, J. G., Alvarez, A. I. and Marques, M. M. (2009). Natural allelic variants of bovine ATP-binding cassette transporter ABCG2: Increased activity of the Ser581 variant and development of tools for the discovery of new ABCG2 inhibitors. Drug Metababolism and Disposition 37, 5-9.
60. Mes, T. H. (2004). Purifying selection and demographic expansion affect sequence diversity of the ligand-binding domain of a glutamate-gated chloride channel gene of Haemonchus placei. Journal of Molecular Evolution 58, 466-478. (Pubitemid 38501420)
61. Mitani, Y., Lezhava, A., Kawai, Y., Kikuchi, T., Oguchi-Katayama, A., Kogo, Y., Itoh, M., Miyagi, T., Takakura, H., Hoshi, K., Kato, C., Arakawa, T., Shibata, K., Fukui, K., Masui, R., Kuramitsu, S., Kiyotani, K., Chalk, A., Tsunekawa, K., Murakami, M., Kamataki, T., Oka, T., Shimada, H., Cizdziel, P. E. and Hayashizaki, Y. (2007). Rapid SNP diagnostics using asymmetric isothermal amplification and a new mismatch-suppression technology. Nature Methods 4, 257-262. (Pubitemid 46358877)
62. Molento, M. B. (2009). Parasite control in the age of drug resistance and changing agricultural practices. Veterinary Parasitology 163, 229-234.
63. Molento, M. B., Wang, G. T. and Prichard, R. K. (1999). Decreased ivermectin and moxidectin sensitivity in Haemonchus contortus selected with moxidectin over 14 generations. Veterinary Parasitology 86, 77-81. (Pubitemid 29387298)
64. Munoz, C., Gomez Talquenca, S. and Volpe, M. L. (2009). Tetra primer ARMS-PCR for identification of SNP in beta-tubulin of Botrytis cinerea, responsible of resistance to benzimidazole. Journal of Microbial Methods 78, 245-246.
65. Neveu, C., Charvet, C., Fauvin, A., Cortet, J., Beech, R. and Cabaret, J. (2010). Genetic diversity of levamisole receptor subunits in parasitic nematodes and abbreviated transcripts associated with resistance. Pharmacogenetics and Genomics 20, 414-425.
66. Njue, A. I. and Prichard, R. K. (2004). Genetic variability of glutamate-gated chloride channel genes in ivermectin-susceptible and -resistant strains of Cooperia oncophora. Parasitology 129, 741-751. (Pubitemid 39657766)
67. Palcy, C., Silvestre, A., Sauve, C., Cortet, J. and Cabaret, J. (2008). Benzimidazole resistance in Trichostrongylus axei in sheep: Long-term monitoring of affected sheep and genotypic evaluation of the parasite. Veterinary Journal 183, 68-74.
68. Puttachary, S., Robertson, A. P., Clark, C. L. and Martin, R. J. (2010). Levamisole and ryanodine receptors. II: An electrophysiological study in Ascaris suum. Molecular and Biochemical Parasitology 171, 8-16.
69. Qian, H., Martin, R. J. and Robertson, A. P. (2006). Pharmacology of N-, L-, and B-subtypes of nematode nAChR resolved at the single-channel level in Ascaris suum. FASEB Journal 20, 2606-2608.
70. Qian, H., Robertson, A. P., Powell-Coffman, J. A. and Martin, R. J. (2008). Levamisole resistance resolved at the single-channel level in Caenorhabditis elegans. FASEB Journal 22, 3247-3254.
71. Rao, V. T., Siddiqui, S. Z., Prichard, R. K. and Forrester, S. G. (2009). A dopamine-gated ion channel (HcGGR3z.ast;) from Haemonchus contortus is expressed in the cervical papillae and is associated with macrocyclic lactone resistance. Molecular and Biochemical Parasitology 166, 54-61.
72. Redman, E., Grillo, V., Saunders, G., Packard, E., Jackson, F., Berriman, M. and Gilleard, J. S. (2008a). Genetics of mating and sex determination in the parasitic nematode Haemonchus contortus. Genetics 180, 1877-1887.
73. Redman, E., Packard, E., Grillo, V., Smith, J., Jackson, F. and Gilleard, J. S. (2008b). Microsatellite analysis reveals marked genetic differentiation between Haemonchus contortus laboratory isolates and provides a rapid system of genetic fingerprinting. International Journal for Parasitology 38, 111-122. (Pubitemid 350262791)
74. Robertson, A. P., Bjorn, H. E. and Martin, R. J. (1999). Resistance to levamisole resolved at the single-channel level. FASEB Journal 13, 749-760. (Pubitemid 29156406)
75. Robertson, A. P., Clark, C. L., Burns, T. A., Thompson, D. P., Geary, T. G., Trailovic, S. M. and Martin, R. J. (2002). Paraherquamide and 2-deoxyparaherquamide distinguish cholinergic receptor subtypes in Ascaris muscle. Journal of Pharmacology and Experimental Therapeutics 302, 853-860. (Pubitemid 34920204)
76. Robertson, A. P., Clark, C. L. and Martin, R. J. (2010). Levamisole and ryanodine receptors. I: A contraction study in Ascaris suum. Molecular and Biochemical Parasitology 171, 1-7.
77. Ronaghi, M., Uhlen, M. and Nyren, P. (1998). A sequencing method based on real-time pyrophosphate. Science 281, 363-365. (Pubitemid 28340773)
78. Rufener, L., Kaminsky, R. and Maser, P. (2009a). In vitro selection of Haemonchus contortus for benzimidazole resistance reveals a mutation at amino acid 198 of beta-tubulin. Molecular and Biochemical Parasitology 168, 120-122.
79. Rufener, L., Maser, P., Roditi, I. and Kaminsky, R. (2009b). Haemonchus contortus acetylcholine receptors of the DEG-3 subfamily and their role in sensitivity to monepantel. PLoS Pathogens 5, e1000380.
80. Saragoza, P. A., Modir, J. G., Goel, N., French, K. L., Li, L., Nowak, M.W. and Stitzel, J. A. (2003). Identification of an alternatively processed nicotinic receptor alpha7 subunit RNA in mouse brain. Brain Research Molecular Brain Research 117, 15-26. (Pubitemid 37123107)
81. Schwenkenbecher, J. M., Albonico, M., Bickle, Q. and Kaplan, R. M. (2007). Characterization of beta-tubulin genes in hookworms and investigation of resistance-associated mutations using real-time PCR. Molecular and Biochemical Parasitology 156, 167-174. (Pubitemid 47600369)
82. Schwenkenbecher, J. M. and Kaplan, R. M. (2009). Real-time PCR assays for monitoring benzimidazole resistance associated mutations in Ancylostoma caninum. Experimental Parasitology 122, 6-10.
83. Silvestre, A. and Cabaret, J. (2002). Mutation in position 167 of isotype 1 beta-tubulin gene of Trichostrongylid nematodes: Role in benzimidazole resistance? Molecular and Biochemical Parasitology 120, 297-300. (Pubitemid 34233794)
84. Silvestre, A. and Humbert, J. F. (2002). Diversity of benzimidazole-resistance alleles in populations of small ruminant parasites. International Journal for Parasitology 32, 921-928. (Pubitemid 34615884)
85. Silvestre, A., Sauve, C., Cortet, J. and Cabaret, J. (2009). Contrasting genetic structures of two parasitic nematodes, determined on the basis of neutral microsatellite markers and selected anthelmintic resistance markers. Molecular Ecology 18, 5086-5100.
86. Sotirchos, I. M., Hudson, A. L., Ellis, J. and Davey, M.W. (2008). Thioredoxins of a parasitic nematode: Comparison of the 16- and 12-kDA thioredoxins from Haemonchus contortus. Free Radical Biology and Medicine 44, 2026-2033.
87. Varady, M., Corba, J., Letkova, V. and Kovac, G. (2009). Comparison of two versions of larval development test to detect anthelmintic resistance in Haemonchus contortus. Veterinary Parasitology 160, 267-271.
88. Von Samson-Himmelstjerna, G., Blackhall, W. J., McCarthy, J. S. and Skuce, P. J. (2007). Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes. Parasitology 134, 1077-1086. (Pubitemid 47026658)
89. Von Samson-Himmelstjerna, G., Walsh, T. K., Donnan, A. A., Carriere, S., Jackson, F., Skuce, P. J., Rohn, K. and Wolstenholme, A. J. (2009). Molecular detection of benzimidazole resistance in Haemonchus contortus using real-time PCR and pyrosequencing. Parasitology 136, 349-358.
90. Walsh, T. K., Donnan, A. A., Jackson, F., Skuce, P. and Wolstenholme, A. J. (2007). Detection and measurement of benzimidazole resistance alleles in Haemonchus contortus using real-time PCR with locked nucleic acid Taqman probes. Veterinary Parasitology 144, 304-312.
91. Webster, L. M., Johnson, P. C., Adam, A., Mable, B. K. and Keller, L. F. (2008) Absence of three known benzimidazole resistance mutations in Trichostrongylus tenuis, a nematode parasite of avian hosts. Veterinary Parasitology 158, 302-310.
92. Williamson, S. M., Robertson, A. P., Brown, L., Williams, T., Woods, D. J., Martin, R. J., Sattelle, D. B. and Wolstenholme, A. J. (2009). The nicotinic acetylcholine receptors of the parasitic nematode Ascaris suum: Formation of two distinct drug targets by varying the relative expression levels of two subunits. PLoS Pathogens 5, e1000517.
93. Ye, S., Dhillon, S., Ke, X., Collins, A. R. and Day, I.N. (2001). An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Research 29, E88-8.