Allozyme analysis of Haemonchus contortus resistant and susceptible to anthelmintics, with an indication of dipeptidases associated with resistance

[1] Anderson, T. J. C., Jaenike, J. (1997): Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology, 115(Part 3): 325–342. DOI: 10.1017/S0031182097001339 http://dx.doi.org/10.1017/S003118209700133910.1017/S0031182097001339Search in Google Scholar

[2] Anderson, T. J., Blouin, M. S., Beech, R. N. (1998): Population biology of parasitic nematodes: applications of genetic markers. Adv. Parasitol., 41: 219–283. DOI: 10.1016/S0065-308X(08)60425-X http://dx.doi.org/10.1016/S0065-308X(08)60425-X10.1016/S0065-308X(08)60425-XSearch in Google Scholar

[3] Andrews, R. H., Chilton, N. B. (1999): Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. Int. J. Parasitol., 29(2): 213–253. DOI: 10.1016/S0020-7519(98) 00168-4 http://dx.doi.org/10.1016/S0020-7519(98)00168-410.1016/S0020-7519(98)00168-4Search in Google Scholar

[4] Beech, R. N., Skuce, P., Bartley, D. J., Martin, R. J., Prichard, R. K., Gilleard, J. S. (2011): Anthelmintic resistance: markers for resistance, or susceptibility? Parasitology, 138(2): 160–174. DOI: 10.1017/S0031182010001198 http://dx.doi.org/10.1017/S003118201000119810.1017/S0031182010001198Search in Google Scholar

[5] Bird, A. F., Bird, J. (1992): The structure of nematodes, San Diego, California, Academic Press, 315 pp. Search in Google Scholar

[6] Blouin, M. S., Yowell, C. A., Courtney, C. H., Dame, J. B. (1997): Haemonchus placei and Haemonchus contortus are distinct species based on mtDNA evidence. Int. J. Parasitol., 27(1): 1383–1387. DOI: 10.1016/S0020-7519(97)00125-2 http://dx.doi.org/10.1016/S0020-7519(97)00125-210.1016/S0020-7519(97)00125-2Search in Google Scholar

[7] Cantacessi, C., Mitreva, M., Campbell, B. E., Hall, R. S., Young, N. D., Jex, A. R., Ranganathan, S., Gasser, R. B. (2010): First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infect. Genet. Evol., 10(8): 1199–1207. DOI: 10.1016/j.meegid.2010.07.024 http://dx.doi.org/10.1016/j.meegid.2010.07.02410.1016/j.meegid.2010.07.024Search in Google Scholar

[8] Cerutti, M. C., Citterio, C. V., Bazzocchi, C., Epis, S., D’amelio, S., Ferrari, N., Lanfranchi P. (2010): Genetic variability of Haemonchus contortus (Nematoda: Trichostrongyloidea) in alpine ruminant host species. J. Helminthol., 84(3): 276–283. DOI: 10.1017/S0022149X09990587 http://dx.doi.org/10.1017/S0022149X0999058710.1017/S0022149X09990587Search in Google Scholar

[9] de Lourdes Mottier, M., Prichard, R. K. (2008): Genetic analysis of a relationship between macrocyclic lactone and benzimidazole anthelmintic selection on Haemonchus contortus. Pharmacogenet. Genom., 2008, 18(2): 129–140. DOI: 10.1097/FPC.0b013e3282f4711d http://dx.doi.org/10.1097/FPC.0b013e3282f4711d10.1097/FPC.0b013e3282f4711dSearch in Google Scholar

[10] Echevarria, F. A., Gennari, S. M., Tait, A. (1992): Isoenzyme analysis of Haemonchus contortus resistant or susceptible to ivermectin. Vet. Parasitol., 44(1–2): 87–95. DOI: 10.1016/0304-4017(92)90146-Z http://dx.doi.org/10.1016/0304-4017(92)90146-Z10.1016/0304-4017(92)90146-ZSearch in Google Scholar

[11] Eng, J. K., Blackhall, W. J., Oseiatweneboana, M. Y., Bourguinat, C., Galazzo, D., Beech, R. N., Unnasch, T. R., Awadzi, K., Lubega, G. W., Prichard, R. K. (2006): Ivermectin selection on betatubulin: evidence in Onchocerca volvulus and Haemonchus contortus. Mol. Biochem. Parasitol., 150(2): 229–235. DOI: 10.1016/j.molbiopara.2006.08.007 http://dx.doi.org/10.1016/j.molbiopara.2006.08.00710.1016/j.molbiopara.2006.08.00717007942Search in Google Scholar

[12] Eysker, M., Bakker, N., Kooyman, F. N., Ploeger, H. W. (2005): The possibilities and limitations of evasive grazing as a control measure for parasitic gastroenteritis in small ruminants in temperate climates. Vet. Parasitol., 129(1–2): 95–104. DOI: 10.1016/j.vetpar.2004.12.022 http://dx.doi.org/10.1016/j.vetpar.2004.12.02210.1016/j.vetpar.2004.12.022Search in Google Scholar

[13] Geldhof, P., Knox, D. (2008): The intestinal contortin structure in Haemonchus contortus: An immobilised anticoagulant? Int. J. Parasitol., 38(13): 1579–1588. DOI: 10.1016/j.ijpara.2008.05.002 http://dx.doi.org/10.1016/j.ijpara.2008.05.00210.1016/j.ijpara.2008.05.002Search in Google Scholar

[14] Grant, W. N. (1994): Genetic variation in parasitic nematodes and its implications. Int. J. Parasitol., 24(6): 821–830. DOI: 10.1016/0020-7519(94)90008-6 http://dx.doi.org/10.1016/0020-7519(94)90008-610.1016/0020-7519(94)90008-6Search in Google Scholar

[15] Grillo, V., Jackson, F., Cabaret, J., Gilleard, J. S. (2007): Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. Int. J. Parasitol., 37(3–4): 435–447. DOI: 10.1016/j.ijpara.2006.11.014 http://dx.doi.org/10.1016/j.ijpara.2006.11.01410.1016/j.ijpara.2006.11.014Search in Google Scholar

[16] Hanzelová, V., Šnábel, V., Kráľová, I., Scholz, T., D’Amelio, S. (1999): Genetic and morphological variability in cestodes of the genus Proteocephalus: geographical variation in P. percae populations. Can. J. Zool., 77(9): 1450–1458. DOI: 10.1139/cjz-77-9-1450 10.1139/cjz-77-9-1450Search in Google Scholar

[17] Hennessy, D. R. (1999): Novel chemical targets. Int. J. Parasitol., 29(1): 113–114. DOI: 10.1016/S0020-7519 (98)00194-5 http://dx.doi.org/10.1016/S0020-7519(98)00194-510.1016/S0020-7519(98)00194-5Search in Google Scholar

[18] Köhler, P. (2001): The biochemical basis of anthelmintic action and resistance. Int. J. Parasitol., 31(4): 336–345. DOI: 10.1016/S0020-7519(01)00131-X http://dx.doi.org/10.1016/S0020-7519(01)00131-X10.1016/S0020-7519(01)00131-XSearch in Google Scholar

[19] Kwa, M. S. G., Kooyman, F. J., Boersema, J. H., Roos, M. H. (1993): Effect of selection for benzimidazole resistance in Haemonchus contortus on β-tubulin isotype 1 and isotype 2 genes. Biochem. Biophys. Res. Commun., 191(2): 413–419. DOI: 10.1006/bbrc.1993.1233 http://dx.doi.org/10.1006/bbrc.1993.123310.1006/bbrc.1993.12338096381Search in Google Scholar

[20] Laurent, V., Brooks, D. R., Coates, D., Isaac, R. E. (2001): Functional expression and characterization of the cytoplasmic aminopeptidase P of Caenorhabditis elegans. Eur. J. Biochem., 268(20): 5430–5438. DOI: 10.1046/ j.0014-2956.2001.02483.x http://dx.doi.org/10.1046/j.0014-2956.2001.02483.x10.1046/j.0014-2956.2001.02483.x11606206Search in Google Scholar

[21] Le Jambre, L. F. (1993): Ivermectin-resistant Haemonchus contortus in Australia. Aust. Vet. J., 70(9): 357. DOI: 10.1111/j.1751-0813.1993.tb00887.x http://dx.doi.org/10.1111/j.1751-0813.1993.tb00887.x10.1111/j.1751-0813.1993.tb00887.x8240179Search in Google Scholar

[22] le Jambre, L. F. (1993): Ivermectin-resistant Haemonchus contortus in Australia. Aust. Vet. J., 70(9): 357. DOI: 10.1111/j.1751-0813.1993.tb00887.x http://dx.doi.org/10.1111/j.1751-0813.1993.tb00887.x10.1111/j.1751-0813.1993.tb00887.xSearch in Google Scholar

[23] Li, B. W., Rush, A. C., Jiang, D. J., Mitreva, M., Abubucker, S., Weil, G. J. (2011): Gender-Associated Genes in Filarial Nematodes Are Important for Reproduction and Potential Intervention. PLoS Negl. Trop. Dis., 5(1), E947–E947. DOI: 10.1371/journal.pntd.0000947 http://dx.doi.org/10.1371/journal.pntd.000094710.1371/journal.pntd.0000947Search in Google Scholar

[24] Murphy, R. W., Sites, Jr. J. W., Buth, D. G., Haufler, C. H. (1996): Proteins: isozyme electrophoresis. In: Hillis, D. M., Moritz, C. (Eds): Molecular Systematics, 2nd ed. Sunderland, Massachusetts: Sinauer Assoc. Inc., pp. 51–120 Search in Google Scholar

[25] Nicoziani, P., Vilhardt, F., Llorente, A., Hilout, L., Courtoy, P. J., Sandvig, K., Van Deurs, B. (2000): Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor. Mol. Biol. Cell., 11(2): 481–495 10.1091/mbc.11.2.481Search in Google Scholar

[26] Otsen, M., Plas, M. E., Groenveld, J., Roos, M. H., Lenstra, J. A., Hoekstra, R. (2000): Genetic markers for the parasitic nematode Haemonchus contortus based on intron sequences. Exp. Parasitol., 95(3): 226–229. DOI: 10.1006/expr.2000.4532 http://dx.doi.org/10.1006/expr.2000.453210.1006/expr.2000.4532Search in Google Scholar

[27] Picamattoccia, L., Novi, A., Cioli, D. (1997): Enzymatic basis for the lack of oxamniquine activity in Schistosoma haematobium infections. Parasitol. Res., 83(7), 687–689. DOI: 10.1007/s004360050320 http://dx.doi.org/10.1007/s00436005032010.1007/s004360050320Search in Google Scholar

[28] R Development Core Team (2010): R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org. Search in Google Scholar

[29] Šnábel, V., de Meeûs, T., Várady, M., Nansen, P., Bjørn, H., Čorba, J. (2000): Sexually linked Mpi locus is presumably involved in imidothiazole resistance in Oesophagostomum dentatum parasites. Parasitol. Res., 86(6): 486–490. DOI: 10.1007/s004360050698 http://dx.doi.org/10.1007/s00436005069810.1007/s004360050698Search in Google Scholar

[30] Sutherland, I. A., Lee, D. L., Lewis D. (1988): Detection of benzimidazole resistance in trichostrongylid nematodes. Parasitol. Today, 4(1): 22–24. DOI: 10.1016/0169-4758(88)90055-5 http://dx.doi.org/10.1016/0169-4758(88)90055-510.1016/0169-4758(88)90055-5Search in Google Scholar

[31] Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011): MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol., 28(10), 2731–2739. DOI: 10.1093/molbev/msr121 http://dx.doi.org/10.1093/molbev/msr12110.1093/molbev/msr121320362621546353Search in Google Scholar

[32] Troell, K., Engström, A., Morrison, D. A., Mattsson, J. G., HÖGLUND, J. (2006): Global patterns reveal strong population structure in Haemonchus contortus, a nematode parasite of domesticated ruminants. Int. J. Parasitol, 36(12), 1305–1316. DOI: 10.1016/j.ijpara.2006.06.015 http://dx.doi.org/10.1016/j.ijpara.2006.06.01510.1016/j.ijpara.2006.06.01516950266Search in Google Scholar

[33] van Wyk, J. A., Malan, F. S. (1988): Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and benzimidazoles in South Africa. Vet. Record, 123(9), 226–228 http://dx.doi.org/10.1136/vr.123.9.22610.1136/vr.123.9.2263176284Search in Google Scholar

[34] Várady, M., Papadopoulos, E., Dolinská, M., KÖnigová, A. (2011): Anthelmintic resistance in parasites of small ruminants: sheep versus goats. Helminthologia, 48(3), 137–144. DOI: 10.2478/s11687-011-0021-7 http://dx.doi.org/10.2478/s11687-011-0021-710.2478/s11687-011-0021-7Search in Google Scholar

[35] Yatsuda, A. P., Krijgsveld, J., Cornelissen, A. W., Heck, A. J., de Vries, E. (2003): Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J. Biol. Chem. 278(19): 16941–16951. DOI: 10.1074/jbc.M212453200 http://dx.doi.org/10.1074/jbc.M21245320010.1074/jbc.M21245320012576473Search in Google Scholar