Structural model, functional modulation by ivermectin and tissue localization of Haemonchus contortus P-glycoprotein-13

Marion David1,2, Chantal Lebrun1, Thomas Duguet2, Franck Talmont3, Robin Beech2, Stéphane Orlowski4, François André4, Roger K. Prichard5, Anne Lespine1
1INTHERES, Université de Toulouse, INRA, ENVT, Toulouse, France
2Institute of Parasitology, McGill University, Sainte-Anne-De-Bellevue, Canada
3Institute of Pharmacology and Structural Biology, UMR 5089, CNRS, Toulouse, France
4CEA, Institut de Biologie Frédéric Joliot, Centre de Saclay, SB2SM, UMR9198 CNRS, I2BC; 91191 Gif-sur-Yvette Cedex, France
5Institute of Parasitology, McGill University, Sainte Anne de Bellevue, Canada

Tài liệu tham khảo

Aller, 2009, Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding, Science, 323, 1718, 10.1126/science.1168750 Andre, 2008, Membrane partitioning of various delta-opioid receptor forms before and after agonist activations: the effect of cholesterol, Biochim. Biophys. Acta, 1778, 1483, 10.1016/j.bbamem.2008.03.017 Ardelli, 2013, Inhibition of P-glycoprotein enhances sensitivity of Caenorhabditis elegans to ivermectin, Vet. Parasitol., 191, 264, 10.1016/j.vetpar.2012.09.021 Bartley, 2009, P-glycoprotein interfering agents potentiate ivermectin susceptibility in ivermectin sensitive and resistant isolates of Teladorsagia circumcincta and Haemonchus contortus, Parasitology, 136, 1081, 10.1017/S0031182009990345 Benkert, 2008, QMEAN: a comprehensive scoring function for model quality assessment, Protein. Struct. Funct. Bioinf., 71, 261, 10.1002/prot.21715 Benkert, 2009, QMEAN server for protein model quality estimation, Nucleic Acids Res., 37, 510, 10.1093/nar/gkp322 Bessadok, 2011, Recognition of sulfonylurea receptor (ABCC8/9) ligands by the multidrug resistance transporter P-glycoprotein (ABCB1): functional similarities based on common structural features between two multispecific ABC proteins, J. Biol. Chem., 286, 3552, 10.1074/jbc.M110.155200 Blaxter, 1996, Nematode spliced leaders-ubiquity, evolution and utility, Int. J. Parasitol., 26, 1025 Brinke, 2013, Effects of a bioassay-derived ivermectin lowest observed effect concentration on life-cycle traits of the nematode Caenorhabditis elegans, Ecotoxicology, 22, 148, 10.1007/s10646-012-1011-3 Campbell, 2016, Ivermectin: a reflection on simplicity (nobel lecture), Angew. Chem. Int. Ed. Engl., 55, 10184, 10.1002/anie.201601492 Corpet, 1988, Multiple sequence alignment with hierarchical clustering, Nucleic Acids Res., 16, 10881, 10.1093/nar/16.22.10881 David, 2016, In silico analysis of the binding of anthelmintics to Caenorhabditis elegans P-glycoprotein 1, Int. J. Parasitol. Drugs Drug Res., 6, 299, 10.1016/j.ijpddr.2016.09.001 Eckford, 2009, ABC efflux pump-based resistance to chemotherapy drugs, Chem. Rev., 109, 2989, 10.1021/cr9000226 Edgar, 2004, MUSCLE: a multiple sequence alignment method with reduced time and space complexity, BMC Bioinf., 5, 113, 10.1186/1471-2105-5-113 Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 32, 1792, 10.1093/nar/gkh340 Freeman, 2003, Amphidial structure of ivermectin-resistant and susceptible laboratory and field strains of Haemonchus contortus, Vet. Parasitol., 110, 217, 10.1016/S0304-4017(02)00321-7 Gallagher, 2016, One-dimensional SDS gel electrophoresis of proteins, Curr. Protoc. Immunol, 1 Garrigues, 2002, Characterization of two pharmacophores on the multidrug transporter P-glycoprotein, Mol. Pharmacol., 62, 288, 10.1124/mol.62.6.1288 Godoy, 2015, Haemonchus contortus P-glycoprotein-2: in situ localisation and characterisation of macrocyclic lactone transport, Int. J. Parasitol., 45, 85, 10.1016/j.ijpara.2014.09.008 Godoy, 2015, Characterization of Haemonchus contortus P-glycoprotein-16 and its interaction with the macrocyclic lactone anthelmintics, Mol. Biochem. Parasitol., 204, 11, 10.1016/j.molbiopara.2015.12.001 Godoy, 2016, Characterisation of P-glycoprotein-9.1 in Haemonchus contortus, Parasit. Vectors, 9, 52, 10.1186/s13071-016-1317-8 Hewitt, 2003, The ABC-transporter signature motif is required for peptide translocation but not peptide binding by TAP, Eur. J. Immunol., 33, 422, 10.1002/immu.200310016 James, 2009, Increased expression of ABC transport proteins is associated with ivermectin resistance in the model nematode Caenorhabditis elegans, Int. J. Parasitol., 39, 213, 10.1016/j.ijpara.2008.06.009 Janssen, 2013, Caenorhabditis elegans: modest increase of susceptibility to ivermectin in individual P-glycoprotein loss-of-function strains, Exp. Parasitol., 134, 171, 10.1016/j.exppara.2013.03.005 Janssen, 2013, Genetic variants and increased expression of Parascaris equorum P-glycoprotein-11 in populations with decreased ivermectin susceptibility, PLoS One, 8, 10.1371/journal.pone.0061635 Janssen, 2015, Transgenically expressed Parascaris P-glycoprotein-11 can modulate ivermectin susceptibility in Caenorhabditis elegans, Int. J. Parasitol. Drugs Drug Resist., 5, 44, 10.1016/j.ijpddr.2015.03.003 Jin, 2012, Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans, Nature, 490, 566, 10.1038/nature11448 Jones, 2005, Multidrug resistance in parasites: ABC transporters, P-glycoproteins and molecular modelling, Int. J. Parasitol., 35, 555, 10.1016/j.ijpara.2005.01.012 Kaplan, 2012, An inconvenient truth: global worming and anthelmintic resistance, Vet. Parasitol., 186, 70, 10.1016/j.vetpar.2011.11.048 Kaschny, 2015, Macrocyclic lactones differ in interaction with recombinant P-glycoprotein 9 of the parasitic nematode Cylicocylus elongatus and ketoconazole in a yeast growth assay, PLoS Pathog., 11, 10.1371/journal.ppat.1004781 Koenderink, 2010, The ABCs of multidrug resistance in malaria, Trends Parasitol., 26, 440, 10.1016/j.pt.2010.05.002 Kolwankar, 2005, Expression and function of ABCB1 and ABCG2 in human placental tissue, Drug Metab. Dispos., 33, 524, 10.1124/dmd.104.002261 Lage, 2003, ABC-transporters: implications on drug resistance from microorganisms to human cancers, Int. J. Antimicrob. Agents, 22, 188, 10.1016/S0924-8579(03)00203-6 Laing, 2013, The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery, Genome Biol., 14, 10.1186/gb-2013-14-8-r88 Lespine, 2007, Interaction of macrocyclic lactones with P-glycoprotein: structure-affinity relationship, Eur. J. Pharm. Sci., 30, 84, 10.1016/j.ejps.2006.10.004 Lespine, 2012, P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance, Int. J. Parasitol. Drugs Drug Resist., 2, 58, 10.1016/j.ijpddr.2011.10.001 Li, 2013, Refined structures of mouse P-glycoprotein, Protein. Sci., 23, 34, 10.1002/pro.2387 Loo, 2001, Defining the drug-binding site in the human multidrug resistance P-glycoprotein using a methanethiosulfonate analog of verapamil, MTS-verapamil, J. Biol. Chem., 276, 14972, 10.1074/jbc.M100407200 Loo, 2002, Location of the rhodamine-binding site in the human multidrug resistance P-glycoprotein, J. Biol. Chem., 277, 44332, 10.1074/jbc.M208433200 Loo, 2006, Transmembrane segment 1 of human P-glycoprotein contributes to the drug-binding pocket, Biochem. J., 396, 537, 10.1042/BJ20060012 Loo, 2006, Transmembrane segment 7 of human P-glycoprotein contributes to the drug-binding pocket, Biochem. J., 399, 351, 10.1042/BJ20060715 Mani, 2016, Interaction of macrocyclic lactones with a Dirofilaria immitis P-glycoprotein, Int. J. Parasitol., 46, 631, 10.1016/j.ijpara.2016.04.004 Menez, 2016, Acquired tolerance to ivermectin and moxidectin after drug selection pressure in the nematode Caenorhabditis elegans, Antimicrob. Agents Chemother., 60, 4809, 10.1128/AAC.00713-16 Morris, 1998, Automated docking using lamarckian genetic algorithm and an empirical binding free energy function, J. Comput. Chem., 19, 1639, 10.1002/(SICI)1096-987X(19981115)19:14<1639::AID-JCC10>3.0.CO;2-B Morris, 2009, AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility, J. Comput. Chem., 30, 2785, 10.1002/jcc.21256 Nakamura, 1997, Function of P-glycoprotein expressed in placenta and mole, Biochem. Biophys. Res. Commun., 235, 849, 10.1006/bbrc.1997.6855 Omasits, 2014, Protter: interactive protein feature visualization and integration with experimental proteomic data, Bioinformatics, 30, 884, 10.1093/bioinformatics/btt607 Pike, 2004, Lipid rafts: heterogeneity on the high seas, Biochem. J., 378, 281, 10.1042/bj20031672 Pouliot, 1997, Reversal of P-glycoprotein-associated multidrug resistance by ivermectin, Biochem. Pharmacol., 53, 17, 10.1016/S0006-2952(96)00656-9 Ranjan, 2002, Selection for resistance to macrocyclic lactones by Haemonchus contortus in sheep, Vet. Parasitol., 103, 109, 10.1016/S0304-4017(01)00551-9 Roulet, 2003, MDR1-deficient genotype in Collie dogs hypersensitive to the P-glycoprotein substrate ivermectin, Eur. J. Pharmacol., 460, 85, 10.1016/S0014-2999(02)02955-2 Sali, 1993, Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol., 234, 779, 10.1006/jmbi.1993.1626 Sarkadi, 1992, Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase, J. Biol. Chem., 267, 4854, 10.1016/S0021-9258(18)42909-2 Sarramegna, 2005, Solubilization, purification, and mass spectrometry analysis of the human mu-opioid receptor expressed in Pichia pastoris, Protein Expr. Purif., 43, 85, 10.1016/j.pep.2005.05.007 Schinkel, 1994, Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs, Cell, 77, 491, 10.1016/0092-8674(94)90212-7 Sharom, 2008, ABC multidrug transporters: structure, function and role in chemoresistance, Pharmacogenomics, 9, 105, 10.2217/14622416.9.1.105 Shilling, 2006, New light on multidrug binding by an ATP-binding-cassette transporter, Trends Pharmacol. Sci., 27, 195, 10.1016/j.tips.2006.02.008 Sippl, 1993, Recognition of errors in three-dimensional structures of proteins, Proteins, 17, 355, 10.1002/prot.340170404 Urdaneta-Marquez, 2014, A dyf-7 haplotype causes sensory neuron defects and is associated with macrocyclic lactone resistance worldwide in the nematode parasite Haemonchus contortus, Int. J. Parasitol., 44, 1063, 10.1016/j.ijpara.2014.08.005 Webb, 2014, Comparative protein structure modeling using MODELLER, Curr. Protoc. Bioinformatics, 47, 1 Wiederstein, 2007, ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins, Nucleic Acids Res., 35, W407, 10.1093/nar/gkm290 Willard, 2003, VADAR: a web server for quantitative evaluation of protein structure quality, Nucleic Acids Res., 31, 3316, 10.1093/nar/gkg565 Ōmura, 2016, Splendid gift from the earth: the origins and impact of the avermectins (nobel lecture), Angew. Chem. Int. Ed., 55, 10190, 10.1002/anie.201602164 Zhao, 2004, Expression analysis of ABC transporters reveals differential functions of tandemly duplicated genes in Caenorhabditis elegans, J. Mol. Biol., 344, 409, 10.1016/j.jmb.2004.09.052