{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T23:20:31Z","timestamp":1787008831650,"version":"build-2736575974"},"reference-count":66,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2022,6,22]],"date-time":"2022-06-22T00:00:00Z","timestamp":1655856000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institute of Health Research","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Natural Science and Engineering Council (NSERC) of Canada to PEM"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,7,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Parasitic nematodes are major human and agricultural pests, and benzimidazoles are amongst the most important broad-spectrum anthelmintic drug class used for their control. Benzimidazole resistance is now widespread in many species of parasitic nematodes in livestock globally and an emerging concern for the sustainable control of human soil-transmitted helminths. \u03b2-tubulin is the major benzimidazole target, although other genes may influence resistance. Among the 6 Caenorhabditis elegans \u03b2-tubulin genes, loss of ben-1 causes resistance without other apparent defects. Here, we explored the genetics of C. elegans \u03b2-tubulin genes in relation to the response to the benzimidazole derivative albendazole. The most highly expressed \u03b2-tubulin isotypes, encoded by tbb-1 and tbb-2, were known to be redundant with each other for viability, and their products are predicted not to bind benzimidazoles. We found that tbb-2 mutants, and to a lesser extent tbb-1 mutants, were hypersensitive to albendazole. The double mutant tbb-2 ben-1 is uncoordinated and short, resembling the wild type exposed to albendazole, but the tbb-1 ben-1 double mutant did not show the same phenotypes. These results suggest that tbb-2 is a modifier of albendazole sensitivity. To better understand how BEN-1 mutates to cause benzimidazole resistance, we isolated mutants resistant to albendazole and found that 15 of 16 mutations occurred in the ben-1 coding region. Mutations ranged from likely nulls to hypomorphs, and several corresponded to residues that cause resistance in other organisms. Null alleles of ben-1 are albendazole-resistant and BEN-1 shows high sequence identity with tubulins from other organisms, suggesting that many amino acid changes could cause resistance. However, our results suggest that missense mutations conferring resistance are not evenly distributed across all possible conserved sites. Independent of their roles in benzimidazole resistance, tbb-1 and tbb-2 may have specialized functions as null mutants of tbb-1 or tbb-2 were cold or heat sensitive, respectively.<\/jats:p>","DOI":"10.1093\/genetics\/iyac093","type":"journal-article","created":{"date-parts":[[2022,6,22]],"date-time":"2022-06-22T10:47:03Z","timestamp":1655894823000},"source":"Crossref","is-referenced-by-count":24,"title":["Interactions of\n                    <i>Caenorhabditis elegans<\/i>\n                    \u03b2-tubulins with the microtubule inhibitor and anthelmintic drug albendazole"],"prefix":"10.1093","volume":"221","author":[{"given":"Linda M","family":"Pallotto","sequence":"first","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4622-8460","authenticated-orcid":false,"given":"Clayton M","family":"Dilks","sequence":"additional","affiliation":[{"name":"Molecular Biosciences, Northwestern University , Evanston, IL 60208, USA"},{"name":"Interdisciplinary Biological Sciences Program, Northwestern University , Evanston, IL 60208, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ye-Jean","family":"Park","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan B","family":"Smit","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian T","family":"Lu","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chandrasekhar","family":"Gopalakrishnan","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6787-4699","authenticated-orcid":false,"given":"John S","family":"Gilleard","sequence":"additional","affiliation":[{"name":"Department of Comparative Biology and Experimental Medicine, Host-Parasite Interactions (HPI) Program, Faculty of Veterinary Medicine, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0229-9651","authenticated-orcid":false,"given":"Erik C","family":"Andersen","sequence":"additional","affiliation":[{"name":"Molecular Biosciences, Northwestern University , Evanston, IL 60208, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4099-4287","authenticated-orcid":false,"given":"Paul E","family":"Mains","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Calgary , Calgary, AB T2N 4N1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,6,22]]},"reference":[{"key":"2022080100015971800_iyac093-B1","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.jmgm.2013.01.007","article-title":"Towards the identification of the binding site of benzimidazoles to beta-tubulin of Trichinella spiralis: insights from computational and experimental data","volume":"41","author":"Aguayo-Ortiz","year":"2013","journal-title":"J Mol Graph Model"},{"issue":"2","key":"2022080100015971800_iyac093-B2","doi-asserted-by":"crossref","first-page":"e1004156","DOI":"10.1371\/journal.pgen.1004156","article-title":"A variant in the neuropeptide receptor npr-1 is a major determinant of Caenorhabditis elegans growth and physiology","volume":"10","author":"Andersen","year":"2014","journal-title":"PLoS Genet"},{"issue":"1","key":"2022080100015971800_iyac093-B3","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.ijpara.2018.10.005","article-title":"Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations","volume":"49","author":"Avramenko","year":"2019","journal-title":"Int J Parasitol"},{"issue":"8","key":"2022080100015971800_iyac093-B4","doi-asserted-by":"crossref","first-page":"e0006606","DOI":"10.1371\/journal.pntd.0006606","article-title":"Toward the 2020 goal of soil-transmitted helminthiasis control and elimination","volume":"12","author":"Becker","year":"2018","journal-title":"PLoS Negl Trop Dis"},{"issue":"1","key":"2022080100015971800_iyac093-B5","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"Brenner","year":"1974","journal-title":"Genetics"},{"issue":"20","key":"2022080100015971800_iyac093-B6","doi-asserted-by":"crossref","first-page":"e193","DOI":"10.1093\/nar\/gkt805","article-title":"Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination","volume":"41","author":"Chen","year":"2013","journal-title":"Nucleic Acids Res"},{"issue":"8","key":"2022080100015971800_iyac093-B7","doi-asserted-by":"crossref","first-page":"2327","DOI":"10.1111\/mec.16400","article-title":"Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands","volume":"31","author":"Crombie","year":"2022","journal-title":"Mol Ecol"},{"key":"2022080100015971800_iyac093-B8","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.50465","article-title":"Deep sampling of Hawaiian Caenorhabditis elegans reveals high genetic diversity and admixture with global populations","volume":"8","author":"Crombie","year":"2019","journal-title":"Elife"},{"key":"2022080100015971800_iyac093-B9","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.ijpddr.2020.08.003","article-title":"Quantitative benzimidazole resistance and fitness effects of parasitic nematode beta-tubulin alleles","volume":"14","author":"Dilks","year":"2020","journal-title":"Int J Parasitol Drugs Drug Resist"},{"key":"2022080100015971800_iyac093-B10","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.ijpddr.2021.09.006","article-title":"Newly identified parasitic nematode beta-tubulin alleles confer resistance to benzimidazoles","volume":"17","author":"Dilks","year":"2021","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"6 Pt 1","key":"2022080100015971800_iyac093-B11","doi-asserted-by":"crossref","first-page":"2993","DOI":"10.1083\/jcb.109.6.2993","article-title":"Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity","volume":"109","author":"Driscoll","year":"1989","journal-title":"J Cell Biol"},{"issue":"Pt 3","key":"2022080100015971800_iyac093-B12","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1242\/jcs.00869","article-title":"Maternally expressed and partially redundant beta-tubulins in Caenorhabditis elegans are autoregulated","volume":"117","author":"Ellis","year":"2004","journal-title":"J Cell Sci"},{"issue":"3","key":"2022080100015971800_iyac093-B13","doi-asserted-by":"crossref","first-page":"e1009297","DOI":"10.1371\/journal.ppat.1009297","article-title":"Two novel loci underlie natural differences in Caenorhabditis elegans abamectin responses","volume":"17","author":"Evans","year":"2021","journal-title":"PLoS Pathog"},{"issue":"2","key":"2022080100015971800_iyac093-B14","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.ijpddr.2018.04.006","article-title":"The transcription factor SKN-1 and detoxification gene ugt-22 alter albendazole efficacy in Caenorhabditis elegans","volume":"8","author":"Fontaine","year":"2018","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"2","key":"2022080100015971800_iyac093-B15","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/0304-4165(80)90431-6","article-title":"Interaction of anthelmintic benzimidazoles with Ascaris suum embryonic tubulin","volume":"630","author":"Friedman","year":"1980","journal-title":"Biochim Biophys Acta"},{"issue":"3","key":"2022080100015971800_iyac093-B16","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1007\/s00436-019-06218-9","article-title":"Albendazole resistance induced in Ancylostoma ceylanicum is not due to single-nucleotide polymorphisms (SNPs) at codons 167, 198, or 200 of the beta-tubulin gene, indicating another resistance mechanism","volume":"118","author":"Furtado","year":"2019","journal-title":"Parasitol Res"},{"issue":"10","key":"2022080100015971800_iyac093-B17","doi-asserted-by":"crossref","first-page":"e0224108","DOI":"10.1371\/journal.pone.0224108","article-title":"First identification of the benzimidazole resistance-associated F200Y SNP in the beta-tubulin gene in Ascaris lumbricoides","volume":"14","author":"Furtado","year":"2019","journal-title":"PLoS One"},{"issue":"3","key":"2022080100015971800_iyac093-B18","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/j.cell.2017.03.046","article-title":"Bacterial metabolism affects the C. elegans response to cancer chemotherapeutics","volume":"169","author":"Garc\u00eda-Gonz\u00e1lez","year":"2017","journal-title":"Cell"},{"key":"2022080100015971800_iyac093-B19","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.ijpddr.2020.09.005","article-title":"Caenorhabditis elegans in anthelmintic research\u2014old model, new perspectives","volume":"14","author":"Hahnel","year":"2020","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"10","key":"2022080100015971800_iyac093-B20","doi-asserted-by":"crossref","first-page":"e1007226","DOI":"10.1371\/journal.ppat.1007226","article-title":"Extreme allelic heterogeneity at a Caenorhabditis elegans beta-tubulin locus explains natural resistance to benzimidazoles","volume":"14","author":"Hahnel","year":"2018","journal-title":"PLoS Pathog"},{"issue":"7","key":"2022080100015971800_iyac093-B21","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1038\/ncb2268","article-title":"Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments","volume":"13","author":"Hao","year":"2011","journal-title":"Nat Cell Biol"},{"key":"2022080100015971800_iyac093-B22","doi-asserted-by":"crossref","first-page":"1652","DOI":"10.1242\/jcs.200923","article-title":"Tubulin isotype substitution revealed that isotype combination modulates microtubule dynamics in C. elegans embryos","volume":"130","author":"Honda","year":"2017","journal-title":"J Cell Sci"},{"issue":"3","key":"2022080100015971800_iyac093-B23","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1534\/genetics.110.116996","article-title":"Specific alpha- and beta-tubulin isotypes optimize the functions of sensory cilia in Caenorhabditis elegans","volume":"185","author":"Hurd","year":"2010","journal-title":"Genetics"},{"key":"2022080100015971800_iyac093-B24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1895\/wormbook.1.182.1","article-title":"Tubulins in C. elegans","volume":"2018","author":"Hurd","year":"2018","journal-title":"WormBook"},{"issue":"1","key":"2022080100015971800_iyac093-B25","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1042\/BJ20141296","article-title":"NHR-176 regulates cyp-35d1 to control hydroxylation-dependent metabolism of thiabendazole in Caenorhabditis elegans","volume":"466","author":"Jones","year":"2015","journal-title":"Biochem J"},{"issue":"3","key":"2022080100015971800_iyac093-B26","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/cm.970220304","article-title":"Amino acid alterations in the benA (beta-tubulin) gene of Aspergillus nidulans that confer benomyl resistance","volume":"22","author":"Jung","year":"1992","journal-title":"Cell Motil Cytoskeleton"},{"issue":"3","key":"2022080100015971800_iyac093-B27","doi-asserted-by":"crossref","first-page":"1173","DOI":"10.1534\/genetics.113.155754","article-title":"Targeted heritable mutation and gene conversion by Cas9-CRISPR in Caenorhabditis elegans","volume":"195","author":"Katic","year":"2013","journal-title":"Genetics"},{"issue":"5","key":"2022080100015971800_iyac093-B28","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/j.ijpara.2018.12.004","article-title":"Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum","volume":"49","author":"Kitchen","year":"2019","journal-title":"Int J Parasitol"},{"key":"2022080100015971800_iyac093-B29","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/bs.apar.2016.02.012","article-title":"Anthelmintic resistance in Haemonchus contortus: history, mechanisms and diagnosis","volume":"93","author":"Kotze","year":"2016","journal-title":"Adv Parasitol"},{"issue":"3","key":"2022080100015971800_iyac093-B30","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.ijpddr.2017.06.001","article-title":"Reduced efficacy of albendazole against Ascaris lumbricoides in Rwandan schoolchildren","volume":"7","author":"Kr\u00fccken","year":"2017","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"2","key":"2022080100015971800_iyac093-B31","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/0166-6851(94)90066-3","article-title":"Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1","volume":"63","author":"Kwa","year":"1994","journal-title":"Mol Biochem Parasitol"},{"issue":"4","key":"2022080100015971800_iyac093-B32","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1006\/jmbi.1994.0102","article-title":"Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans","volume":"246","author":"Kwa","year":"1995","journal-title":"J Mol Biol"},{"issue":"2\u20133","key":"2022080100015971800_iyac093-B33","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/0001-706X(94)90066-3","article-title":"Biochemistry of benzimidazole resistance","volume":"56","author":"Lacey","year":"1994","journal-title":"Acta Trop"},{"issue":"2","key":"2022080100015971800_iyac093-B34","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/0166-6851(86)90122-2","article-title":"Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus","volume":"19","author":"Lacey","year":"1986","journal-title":"Mol Biochem Parasitol"},{"issue":"4","key":"2022080100015971800_iyac093-B35","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1091\/mbc.E20-07-0492","article-title":"Epistatic, synthetic, and balancing interactions among tubulin missense mutations affecting neurite growth in Caenorhabditis elegans","volume":"32","author":"Lee","year":"2021","journal-title":"Mol Biol Cell"},{"issue":"8","key":"2022080100015971800_iyac093-B36","doi-asserted-by":"crossref","first-page":"1228","DOI":"10.1002\/ps.3680","article-title":"Detection and dynamics of different carbendazim-resistance conferring beta-tubulin variants of Gibberella zeae collected from infected wheat heads and rice stubble in China","volume":"70","author":"Liu","year":"2014","journal-title":"Pest Manag Sci"},{"issue":"1","key":"2022080100015971800_iyac093-B37","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1534\/genetics.104.030106","article-title":"Mutations of a redundant \u03b1-tubulin gene affect Caenorhabditis elegans early embryonic cleavage via MEI-1\/katanin-dependent and -independent pathways","volume":"170","author":"Lu","year":"2005","journal-title":"Genetics"},{"issue":"1","key":"2022080100015971800_iyac093-B38","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1091\/mbc.e03-06-0418","article-title":"The Caenorhabditis elegans microtubule-severing complex MEI-1\/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotypes","volume":"15","author":"Lu","year":"2004","journal-title":"Mol Biol Cell"},{"key":"2022080100015971800_iyac093-B39","first-page":"136","author":"Lu","year":"2004"},{"key":"2022080100015971800_iyac093-B40","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0074-7696(08)62138-5","article-title":"Multiple forms of tubulin: different gene products and covalent modifications","volume":"178","author":"Luduena","year":"1998","journal-title":"Int Rev Cytol"},{"issue":"2","key":"2022080100015971800_iyac093-B41","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1093\/genetics\/125.2.351","article-title":"Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans","volume":"125","author":"Mains","year":"1990","journal-title":"Genetics"},{"issue":"3","key":"2022080100015971800_iyac093-B42","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1016\/j.ijpddr.2018.09.005","article-title":"UDP-glycosyltransferase family in Haemonchus contortus: phylogenetic analysis, constitutive expression, sex-differences and resistance-related differences","volume":"8","author":"Matou\u0161kov\u00e1","year":"2018","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"1","key":"2022080100015971800_iyac093-B43","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1186\/s13071-020-3978-6","article-title":"New codon 198 \u03b2-tubulin polymorphisms in highly benzimidazole resistant Haemonchus contortus from goats in three different states in Sudan","volume":"13","author":"Mohammedsalih","year":"2020","journal-title":"Parasit Vectors"},{"key":"2022080100015971800_iyac093-B44","doi-asserted-by":"crossref","first-page":"j4307","DOI":"10.1136\/bmj.j4307","article-title":"Efficacy of recommended drugs against soil transmitted helminths: systematic review and network meta-analysis","volume":"358","author":"Moser","year":"2017","journal-title":"BMJ"},{"issue":"1","key":"2022080100015971800_iyac093-B45","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1247\/csf.21022","article-title":"Expression patterns and levels of all tubulin isotypes analyzed in GFP knock-in C. elegans strains","volume":"46","author":"Nishida","year":"2021","journal-title":"Cell Struct Funct"},{"issue":"6638","key":"2022080100015971800_iyac093-B46","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/40618","article-title":"Evolution of genetic redundancy","volume":"388","author":"Nowak","year":"1997","journal-title":"Nature"},{"issue":"8","key":"2022080100015971800_iyac093-B47","doi-asserted-by":"crossref","first-page":"e0252000","DOI":"10.1371\/journal.pone.0252000","article-title":"easyXpress: an R package to analyze and visualize high-throughput C. elegans microscopy data generated using CellProfiler","volume":"16","author":"Nyaanga","year":"2021","journal-title":"PLoS One"},{"issue":"2","key":"2022080100015971800_iyac093-B48","doi-asserted-by":"crossref","first-page":"351","DOI":"10.4269\/ajtmh.18-0727","article-title":"Genetic markers of benzimidazole resistance among human hookworms (Necator americanus) in Kintampo North Municipality, Ghana","volume":"100","author":"Orr","year":"2019","journal-title":"Am J Trop Med Hyg"},{"issue":"4","key":"2022080100015971800_iyac093-B49","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1093\/genetics\/113.4.821","article-title":"Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans","volume":"113","author":"Park","year":"1986","journal-title":"Genetics"},{"issue":"2","key":"2022080100015971800_iyac093-B50","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1002\/cm.20003","article-title":"Roles for two partially redundant alpha-tubulins during mitosis in early Caenorhabditis elegans embryos","volume":"58","author":"Phillips","year":"2004","journal-title":"Cell Motil Cytoskeleton"},{"issue":"2","key":"2022080100015971800_iyac093-B51","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1002\/ddr.21933","article-title":"Benzimidazole-carbamate anthelmintics: perspective candidates for the anticancer drug development","volume":"83","author":"Prasher","year":"2022","journal-title":"Drug Dev Res"},{"issue":"2","key":"2022080100015971800_iyac093-B52","doi-asserted-by":"crossref","first-page":"e0003494","DOI":"10.1371\/journal.pntd.0003494","article-title":"The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps","volume":"9","author":"Redman","year":"2015","journal-title":"PLoS Negl Trop Dis"},{"issue":"1","key":"2022080100015971800_iyac093-B53","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1091\/mbc.5.1.29","article-title":"Systematic mutational analysis of the yeast beta-tubulin gene","volume":"5","author":"Reijo","year":"1994","journal-title":"Mol Biol Cell"},{"key":"2022080100015971800_iyac093-B54","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1051\/parasite\/2020062","article-title":"Increasing importance of anthelmintic resistance in European livestock: creation and meta-analysis of an open database","volume":"27","author":"Rose Vineer","year":"2020","journal-title":"Parasite"},{"issue":"6","key":"2022080100015971800_iyac093-B55","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1016\/j.ijpara.2012.12.011","article-title":"Characterization and comparative analysis of the complete Haemonchus contortus beta-tubulin gene family and implications for benzimidazole resistance in strongylid nematodes","volume":"43","author":"Saunders","year":"2013","journal-title":"Int J Parasitol"},{"issue":"7","key":"2022080100015971800_iyac093-B56","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat Methods"},{"issue":"7","key":"2022080100015971800_iyac093-B57","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.pt.2018.04.008","article-title":"Preventive chemotherapy in the fight against soil-transmitted helminthiasis: achievements and limitations","volume":"34","author":"Schulz","year":"2018","journal-title":"Trends Parasitol"},{"issue":"11","key":"2022080100015971800_iyac093-B58","doi-asserted-by":"crossref","first-page":"2616","DOI":"10.1139\/z82-336","article-title":"The effects of mebendazole on the growth and development of Caenorhabditis elegans","volume":"60","author":"Spence","year":"1982","journal-title":"Can J Zool"},{"key":"2022080100015971800_iyac093-B59","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.ijpddr.2019.09.001","article-title":"Similarities and differences in the biotransformation and transcriptomic responses of Caenorhabditis elegans and Haemonchus contortus to five different benzimidazole drugs","volume":"11","author":"Stasiuk","year":"2019","journal-title":"Int J Parasitol Drugs Drug Resist"},{"issue":"4","key":"2022080100015971800_iyac093-B60","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1093\/genetics\/111.4.715","article-title":"Isolation and characterization of mutations in the beta-tubulin gene of Saccharomyces cerevisiae","volume":"111","author":"Thomas","year":"1985","journal-title":"Genetics"},{"issue":"10","key":"2022080100015971800_iyac093-B61","doi-asserted-by":"crossref","first-page":"1749","DOI":"10.1101\/gr.157651.113","article-title":"The Million Mutation Project: a new approach to genetics in Caenorhabditis elegans","volume":"23","author":"Thompson","year":"2013","journal-title":"Genome Res"},{"key":"2022080100015971800_iyac093-B62","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.pt.2020.11.008","article-title":"Complementary approaches with free-living and parasitic nematodes to understanding anthelmintic resistance","volume":"37","author":"Wit","year":"2020","journal-title":"Trends Parasitol"},{"key":"2022080100015971800_iyac093-B63","author":"World Health Organization","year":"2015"},{"key":"2022080100015971800_iyac093-B64","first-page":"589","article-title":"Summary of global update on preventive chemotherapy implementation in 2016: crossing the billion","volume":"92","author":"World Health Organization","year":"2017","journal-title":"Wkly Epidemiol Rec"},{"issue":"11","key":"2022080100015971800_iyac093-B65","doi-asserted-by":"crossref","first-page":"4512","DOI":"10.1091\/mbc.e03-01-0017","article-title":"Mutations in a beta-tubulin disrupt spindle orientation and microtubule dynamics in the early Caenorhabditis elegans embryo","volume":"14","author":"Wright","year":"2003","journal-title":"Mol Biol Cell"},{"issue":"3","key":"2022080100015971800_iyac093-B66","doi-asserted-by":"crossref","first-page":"e0006368","DOI":"10.1371\/journal.pntd.0006368","article-title":"Discovery of genomic intervals that underlie nematode responses to benzimidazoles","volume":"12","author":"Zamanian","year":"2018","journal-title":"PLoS Negl Trop Dis"}],"container-title":["Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/advance-article-pdf\/doi\/10.1093\/genetics\/iyac093\/44409303\/iyac093.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/221\/4\/iyac093\/45196247\/iyac093.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/221\/4\/iyac093\/45196247\/iyac093.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,27]],"date-time":"2024-09-27T10:20:15Z","timestamp":1727432415000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/doi\/10.1093\/genetics\/iyac093\/6613138"}},"subtitle":[],"editor":[{"given":"B","family":"Goldstein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,6,22]]},"references-count":66,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,6,22]]},"published-print":{"date-parts":[[2022,7,30]]}},"URL":"https:\/\/doi.org\/10.1093\/genetics\/iyac093","relation":{},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,8,1]]},"published":{"date-parts":[[2022,6,22]]},"article-number":"iyac093"}}