In vitro selection of Giardia duodenalis for Albendazole resistance identifies a β-tubulin mutation at amino acid E198K

Samantha J. Emery-Corbin1,2, Qiao Su1,2, Swapnil Tichkule1,2, Louise Baker1,2, Ernest Lacey3,4, Aaron R. Jex1,5,2
1Population Health and Immunity Division, The Walter and Eliza Hall Institute of Medical Research, Melbourne, VIC, Australia
2Department of Medical Biology, The University of Melbourne, Parkville, VIC, Australia
3Microbial Screening Technologies, Smithfield, NSW, Australia
4Department of Chemistry and Biomolecular Sciences, Faculty of Science, Macquarie University, North Ryde, NSW, Australia
5Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, Australia

Tài liệu tham khảo

Agarwal, 1993, Segregation of activity profile in benzimidazoles: effect of spacers at 5(6)-position of methyl benzimidazole-2-carbamates [1], Z. Naturforsch. C Biosci., 48, 829, 10.1515/znc-1993-11-1203

Aguayo-Ortiz, 2013, Towards the identification of the binding site of benzimidazoles to beta-tubulin of Trichinella spiralis: insights from computational and experimental data, J. Mol. Graph. Model., 41, 12, 10.1016/j.jmgm.2013.01.007

Aguayo-Ortiz, 2013, Molecular basis for benzimidazole resistance from a novel β-tubulin binding site model, J. Mol. Graph. Model., 45, 26, 10.1016/j.jmgm.2013.07.008

Ansell, 2017, Transcriptomics indicates active and passive metronidazole resistance mechanisms in three seminal giardia lines, Front. Microbiol., 8, 398, 10.3389/fmicb.2017.00398

Ansell, 2015, Drug resistance in Giardia duodenalis, Biotechnol. Adv., 33, 888, 10.1016/j.biotechadv.2015.04.009

Ansell, 2019, Annotation of the Giardia proteome through structure-based homology and machine learning, GigaScience, 8, 10.1093/gigascience/giy150

Argüello-García, 2015, An antioxidant response is involved in resistance of Giardia duodenalis to albendazole, Front. Microbiol., 6, 10.3389/fmicb.2015.00286

Arguello-Garcia, 2009, In vitro resistance to 5-nitroimidazoles and benzimidazoles in Giardia duodenalis: variability and variation in gene expression, Infect. Genet. Evol., 9, 1057, 10.1016/j.meegid.2009.05.015

Aubrey, 2015, An inducible lentiviral guide RNA platform enables the identification of tumor-essential genes and tumor-promoting mutations in vivo, Cell Rep., 10, 1422, 10.1016/j.celrep.2015.02.002

Banno, 2008, Genotyping of benzimidazole-resistant and dicarboximide-resistant mutations in Botrytis cinerea using real-time polymerase chain reaction assays, Phytopathology, 98, 397, 10.1094/PHYTO-98-4-0397

Barrett, 2019, Protozoan persister-like cells and drug treatment failure, Nat. Rev. Microbiol., 17, 607, 10.1038/s41579-019-0238-x

Beech, 2011, Anthelmintic resistance: markers for resistance, or susceptibility?, Parasitology, 138, 160, 10.1017/S0031182010001198

Boreham, 1984, The sensitivity of Giardia intestinalis to drugs in vitro, J. Antimicrob. Chemother., 14, 449, 10.1093/jac/14.5.449

Cai, 2015, M233I mutation in the beta-tubulin of Botrytis cinerea confers resistance to zoxamide, Sci. Rep., 5, 10.1038/srep16881

Capon, 1989, Similarities of Giardia antigens derived from human and animal sources, Int. J. Parasitol., 19, 91, 10.1016/0020-7519(89)90026-X

Chatterji, 2011, Microtubules as antifungal and antiparasitic drug targets, Expert Opin. Ther. Pat., 21, 167, 10.1517/13543776.2011.545349

Chavez, 1992, Giardia lamblia: ultrastructural study of the in vitro effect of benzimidazoles, J. Protozool., 39, 510, 10.1111/j.1550-7408.1992.tb04841.x

Davids, 2011, 381

Dayan, 2003, Albendazole, mebendazole and praziquantel. Review of non-clinical toxicity and pharmacokinetics, Acta Trop., 86, 141, 10.1016/S0001-706X(03)00031-7

Edlind, 1990, Activity of the anthelmintic benzimidazoles against Giardia lamblia in vitro, J. Infect. Dis., 162, 1408, 10.1093/infdis/162.6.1408

Emery, 2018, Differential protein expression and post-translational modifications in metronidazole-resistant Giardia duodenalis, GigaScience, 7, 10.1093/gigascience/giy024

Ghisi, 2007, Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes, Vet. Parasitol., 144, 313, 10.1016/j.vetpar.2006.10.003

Hanevik, 2014, Irritable bowel syndrome and chronic fatigue 6 years after giardia infection: a controlled prospective cohort study, Clin. Infect. Dis., 59, 1394, 10.1093/cid/ciu629

Hennessey, 2020, Nek8445, a protein kinase required for microtubule regulation and cytokinesis in Giardia lamblia, Mol. Biol. Cell, 31, 1611, 10.1091/mbc.E19-07-0406

Hunskar, 2016, Excessive daytime sleepiness, sleep need and insomnia 3 years after Giardia infection: a cohort study, Sleep Health, 2, 154, 10.1016/j.sleh.2016.03.005

Katiyar, 1994, Antiprotozoal activities of benzimidazoles and correlations with beta-tubulin sequence, Antimicrob. Agents Chemother., 38, 2086, 10.1128/AAC.38.9.2086

Keeling, 1996, Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family, Mol. Biol. Evol., 13, 1297, 10.1093/oxfordjournals.molbev.a025576

Lacey, 1988, The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles, Int. J. Parasitol., 18, 885, 10.1016/0020-7519(88)90175-0

Lacey, 1986, Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus, Mol. Biochem. Parasitol., 19, 171, 10.1016/0166-6851(86)90122-2

Lalle, 2018, Treatment-refractory giardiasis: challenges and solutions, Infect. Drug Resist., 11, 1921, 10.2147/IDR.S141468

Lane, 2002, Current trends in research into the waterborne parasite Giardia, Crit. Rev. Microbiol., 28, 123, 10.1080/1040-840291046713

Lemee, 2000, Metronidazole and albendazole susceptibility of 11 clinical isolates of Giardia duodenalis from France, J. Antimicrob. Chemother., 46, 819, 10.1093/jac/46.5.819

Leroux, 1999, Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards, Crop Protect., 18, 687, 10.1016/S0261-2194(99)00074-5

Lindquist, 1996, Induction of albendazole resistance in Giardia lamblia, Microb. Drug Resist., 2, 433, 10.1089/mdr.1996.2.433

Litleskare, 2018, Prevalence of irritable bowel syndrome and chronic fatigue 10 Years after giardia infection, Clin. Gastroenterol. Hepatol., 16, 1064, 10.1016/j.cgh.2018.01.022

Mariante, 2005, Giardia lamblia: evaluation of the in vitro effects of nocodazole and colchicine on trophozoites, Exp. Parasitol., 110, 62, 10.1016/j.exppara.2005.01.007

McLoughlin, 2020, Colchicine-binding site inhibitors from chemistry to clinic: a review, Pharmaceuticals, 13, 10.3390/ph13010008

Meltzer, 2014, Treatment of giardiasis after nonresponse to nitroimidazole, Emerg. Infect. Dis., 20, 1742, 10.3201/eid2010.140073

Morgan, 1993, Activities of several benzimidazoles and tubulin inhibitors against Giardia spp. in vitro, Antimicrob. Agents Chemother., 37, 328, 10.1128/AAC.37.2.328

Robinson, 2004, A possible model of benzimidazole binding to beta-tubulin disclosed by invoking an inter-domain movement, J. Mol. Graph. Model., 23, 275, 10.1016/j.jmgm.2004.08.001

Russell, 1992, Binding of [3H]benzimidazole carbamates to mammalian brain tubulin and the mechanism of selective toxicity of the benzimidazole anthelmintics, Biochem. Pharmacol., 43, 1095, 10.1016/0006-2952(92)90617-R

Schonbrunn, 1999, Crystallization of a macromolecular ring assembly of tubulin liganded with the anti-mitotic drug podophyllotoxin, J. Struct. Biol., 128, 211, 10.1006/jsbi.1999.4183

Solaymani-Mohammadi, 2010, A meta-analysis of the effectiveness of albendazole compared with metronidazole as treatments for infections with Giardia duodenalis, PLoS Neglected Trop. Dis., 4, 10.1371/journal.pntd.0000682

Townson, 1992, Induction of metronidazole and furazolidone resistance in Giardia, Trans. R. Soc. Trop. Med. Hyg., 86, 521, 10.1016/0035-9203(92)90095-T

Upcroft, 1996, Albendazole resistance in Giardia is correlated with cytoskeletal changes but not with a mutation at amino acid 200 in beta-tubulin, Microb. Drug Resist., 2, 303, 10.1089/mdr.1996.2.303

Van der Auwera, 2013, From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline, Curr Protoc Bioinformatics, 43, 10.1002/0471250953.bi1110s43

Vela-Corcía, 2018, Analysis of β-tubulin-carbendazim interaction reveals that binding site for MBC fungicides does not include residues involved in fungicide resistance, Sci. Rep., 8, 7161, 10.1038/s41598-018-25336-5

Wang, 2016, Structures of a diverse set of colchicine binding site inhibitors in complex with tubulin provide a rationale for drug discovery, FEBS J., 283, 102, 10.1111/febs.13555

Yang, 2013, BioLiP: a semi-manually curated database for biologically relevant ligand-protein interactions, Nucleic Acids Res., 41, D1096, 10.1093/nar/gks966

Yarden, 1993, Mutations leading to substitutions at amino acids 198 and 200 of beta-tubulin that correlate with benomyl-resistance phenotypes of field strains of Botrytis cinerea, Phytopathology, 83, 1478, 10.1094/Phyto-83-1478