Profiling G protein-coupled receptors of Fasciola hepatica identifies orphan rhodopsins unique to phylum Platyhelminthes

Abunna, 2010, Bovine fasciolosis: coprological, abattoir survey and its economic impact due to liver condemnation at Soddo municipal abattoir, Southern Ethiopia, Trop. Anim. Health Prod., 42, 289, 10.1007/s11250-009-9419-3 Åkerberg, 2010, Mutagenesis of human neuropeptide Y/peptide YY receptor Y2 reveals additional differences to Y1 in interactions with highly conserved ligand positions, Regul. Pept., 163, 120, 10.1016/j.regpep.2010.04.011 Altschul, 1990, Basic local alignment search tool, J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 Ayers, 2010, Evaluating smoothened as a G-protein-coupled receptor for hedgehog signalling, Trends Cell Biol., 20, 287, 10.1016/j.tcb.2010.02.002 Babicki, 2016, Heatmapper: web-enabled heat mapping for all, Nucleic Acids Res., 44, W147, 10.1093/nar/gkw419 Berglund, 2002, Reciprocal mutations of neuropeptide Y receptor Y2 in human and chicken identify amino acids important for antagonist binding, FEBS Lett., 518, 5, 10.1016/S0014-5793(02)02534-6 Buxton, 2011, On the mode of action of emodepside: slow effects on membrane potential and voltage-activated currents in Ascaris suum, Br. J. Pharmacol., 164, 453, 10.1111/j.1476-5381.2011.01428.x Cabada, 2016, Treatment failure after multiple courses of triclabendazole among patients with fasciolosis in Cusco, Peru: a case series, PLoS Neglected Trop. Dis., 10, 10.1371/journal.pntd.0004361 Camacho, 2008, BLAST+: architecture and applications, BMC Bioinf., 10, 421, 10.1186/1471-2105-10-421 Campos, 2014, Identification of G protein-coupled receptors in Schistosoma haematobium and S. mansoni by comparative genomics, Parasites Vectors, 7, 242, 10.1186/1756-3305-7-242 Collins, 2010, Genome-wide analyses reveal a role for peptide hormones in planarian germline development, PLoS Biol., 8, 10.1371/journal.pbio.1000509 Collins, 2013, Adult somatic stem cells in the human parasite Schistosoma mansoni, Nature, 494, 476, 10.1038/nature11924 Crooks, 2004, WebLogo: a sequence logo generator, Genome Res., 14, 1188, 10.1101/gr.849004 Cwiklinski, 2015, The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution, Genome Biol., 16, 71, 10.1186/s13059-015-0632-2 Dell'Oca, 2014, RNA interference in Fasciola hepatica newly excysted juveniles: long dsRNA induces more persistent silencing than siRNA, Mol. Biochem. Parasitol., 197, 28, 10.1016/j.molbiopara.2014.10.001 Dereeper, 2008, Phylogeny.fr: robust phylogenetic analysis for the non-specialist, Nucleic Acids Res., 36, W465, 10.1093/nar/gkn180 Fällmar, 2011, Identification of positions in the human neuropeptide Y/peptide YY receptor Y2 that contribute to pharmacological differences between receptor subtypes, Neuropeptides, 45, 293, 10.1016/j.npep.2011.05.006 Finn, 2015, HMMER web server: 2015 update, Nucleic Acids Res., 43, W30, 10.1093/nar/gkv397 Fredriksson, 2003, The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints, Mol. Pharmacol., 63, 1256, 10.1124/mol.63.6.1256 Galvez, 2000, Mapping the agonist binding site of GABAB type 1 subunit sheds light on the activation process of GABAB receptors, J. Biol. Chem., 275, 41166, 10.1074/jbc.M007848200 Gehrke, 2016, Neoblasts and the evolution of whole-body regeneration, Curr. Opin. Genet. Dev., 40, 131, 10.1016/j.gde.2016.07.009 Geng, 2013, Structural mechanism of ligand activation in human GABA(B) receptor, Nature, 504, 254, 10.1038/nature12725 Gurley, 2008, Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis, Science, 319, 323, 10.1126/science.1150029 Habarugira, 2016, Pathological findings of condemned bovine liver specimens and associated economic loss at Nyabugogo abattoir, Kigali, Rwanda, Acta Trop., 164, 27, 10.1016/j.actatropica.2016.07.020 Harder, 2003, Cyclooctadepsipeptides – an anthelmintically active class of compounds exhibiting a novel mode of action, Int. J. Antimicrob. Agents, 22, 318, 10.1016/S0924-8579(03)00219-X Hirashima, 2008, Homology modeling, agonist binding site identification, and docking in octopamine receptor of Periplaneta americana, Comput. Biol. Chem., 32, 185, 10.1016/j.compbiolchem.2008.03.001 Hotez, 2008, Helminth infections: the great neglected tropical diseases, J. Clin. Invest., 118, 1311, 10.1172/JCI34261 Howe, 2017, WormBase ParaSite – a comprehensive resource for helminth genomics, Mol. Biochem. Parasitol., 215, 2, 10.1016/j.molbiopara.2016.11.005 Howell, 2015, Epidemiology and impact of Fasciola hepatica exposure in high-yielding dairy herds, Prev. Vet. Med., 121, 41, 10.1016/j.prevetmed.2015.05.013 Huang, 2007, Identification of critical structural determinants responsible for octopamine binding to the alpha-adrenergic-like Bombyx mori octopamine receptor, Biochemistry, 46, 5896, 10.1021/bi602593t Janda, 2012, Structural basis of wnt recognition by frizzled, Science, 337, 59, 10.1126/science.1222879 Jiang, 2011, Synthetic spike-in standards for RNA-Seq experiments, Genome Res., 21, 1543, 10.1101/gr.121095.111 Jones, 2014, InterProScan 5: genome-scale protein function classification, Bioinformatics, 30, 1236, 10.1093/bioinformatics/btu031 Kalani, 2004, The predicted 3D structure of the human D2 dopamine receptor and the binding site and binding affinities for agonists and antagonists, Proc. Natl. Acad. Sci. U.S.A., 101, 3815, 10.1073/pnas.0400100101 Katoh, 2017, MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization, Briefings Bioinf. Kelley, 2016, Current threat of triclabendazole resistance in Fasiola hepatica, Trends Parasitol., 32, 458, 10.1016/j.pt.2016.03.002 Khalturin, 2009, More than just orphans: are taxonomically-restricted genes important in evolution?, Trends Genet., 25, 404, 10.1016/j.tig.2009.07.006 Koziol, 2014, The unique stem cell system of the immortal larvae of the human parasite Echinococcus multilocularis, EvoDevo, 5, 10, 10.1186/2041-9139-5-10 Koziol, 2016, De novo discovery of neuropeptides in the genomes of parasitic flatworms using a novel comparative approach, Int. J. Parasitol., 46, 709, 10.1016/j.ijpara.2016.05.007 Kruse, 2012, Structure and dynamics of the M3 muscarinic acetylcholine receptor, Nature, 482, 552, 10.1038/nature10867 Kumar, 2016, MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054 Lagerström, 2008, Structural diversity of G protein-coupled receptors and significance for drug discovery, Nat. Rev. Drug Discov., 7, 339, 10.1038/nrd2518 Langenhan, 2013, Sticky signaling – adhesion class G protein-coupled receptors take the stage, Sci. Signal., 6, 10.1126/scisignal.2003825 Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol., 10, R25, 10.1186/gb-2009-10-3-r25 Li, 2010, Wnt4, the first member of the Wnt family identified in Schistosoma japonicum, regulates worm development by the canonical pathway, Parasitol. Res., 107, 795, 10.1007/s00436-010-1933-8 Lowery, D.E., Geary, T.G., Kubiak, T.M., Larsen, M.J., 2003. G protein-coupled receptor-like receptors and modulators thereof. Pharmacia and Upjohn Company, United States. Patent US 6632621 B1. MacDonald, 2016, A constitutively active G protein-coupled acetylcholine receptor regulates motility of larval Schistosoma mansoni, Mol. Biochem. Parasitol., 202, 29, 10.1016/j.molbiopara.2015.09.001 Martin, 2010, Control of nematode parasites with agents acting on neuro-musculature systems: lessons for neuropeptide ligand discovery, Adv. Exp. Med. Biol., 692, 138, 10.1007/978-1-4419-6902-6_7 Martin-Duran, 2017, Increased taxon sampling reveals thousands of hidden orthologs in flatworms, Genome Res., 27, 1263, 10.1101/gr.216226.116 McCammick, 2016, Calmodulin disruption impacts growth and motility in juvenile liver fluke, Parasites Vectors, 9, 46, 10.1186/s13071-016-1324-9 McCusker, 2016, Stimulating neoblast-like cell proliferation in juvenile Fasciola hepatica supports growth and progression towards the adult phenotype in vitro, PLoS Neglected Trop. Dis., 10, 10.1371/journal.pntd.0004994 McGonigle, 2008, The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduced gut penetration, Int. J. Parasitol., 38, 149, 10.1016/j.ijpara.2007.10.007 McNulty, 2017, Genomes of Fasciola hepatica from the Americas reveal colonization with Neorickettsia endobacteria related to the agents of Potomac horse and human sennetsu fevers, PLoS Genet., 13, 10.1371/journal.pgen.1006537 McVeigh, 2017 McVeigh, 2009, Discovery of multiple neuropeptide families in the phylum Platyhelminthes, Int. J. Parasitol., 39, 1243, 10.1016/j.ijpara.2009.03.005 McVeigh, 2012, Parasite neuropeptide biology: seeding rational drug target selection?, Int. J. Parasitol.: Drugs Drug. Res., 2, 76 McVeigh, 2014, RNAi dynamics in juvenile Fasciola spp. liver flukes reveals the persistence of gene silencing in vitro, PLoS Neglected Trop. Dis., 8, 10.1371/journal.pntd.0003185 Mendonça-Silva, 2004, Characterization of a GABAergic neurotransmission in adult Schistosoma mansoni, Parasitology, 129, 137, 10.1017/S0031182004005554 Mitri, 2004, Divergent evolution in metabotropic glutamate receptors. A new receptor activated by an endogenous ligand different from glutamate in insects, J. Biol. Chem., 279, 9313, 10.1074/jbc.M310878200 Mousley, 2004, Arthropod FMRFamide-related peptides modulate muscle activity in helminths, Int. J. Parasitol., 34, 755, 10.1016/j.ijpara.2004.02.005 Mousley, 2005, Expression and bioactivity of allatostatin-like neuropeptides in helminths, Int. J. Parasitol., 35, 1557, 10.1016/j.ijpara.2005.08.002 Nakamura, 2015, Applications of yeast-based signaling sensor for characterization of antagonist and analysis of site-directed mutants of the human serotonin 1A receptor, Biotechnol. Bioeng., 112, 1906, 10.1002/bit.25597 Nishimura, 2008, Characterization of tyramine beta-hydroxylase in planarian Dugesia japonica: cloning and expression, Neurochem. Int., 53, 184, 10.1016/j.neuint.2008.09.006 Nishimura, 2009, Identification of a novel planarian G-protein-coupled receptor that responds to serotonin in Xenopus laevis oocytes, Biol. Pharm. Bull., 32, 1672, 10.1248/bpb.32.1672 Omar, 2007, Identification of a platyhelminth neuropeptide receptor, Int. J. Parasitol., 37, 725, 10.1016/j.ijpara.2006.12.019 Orhan, 2013, Further insights into GPR179: expression, localization and associated pathogenic mechanisms leading to complete congenital stationary night blindness, Invest. Ophthalmol. Vis. Sci., 54, 8041, 10.1167/iovs.13-12610 Orlandi, 2013, GPR158 and GPR179: a subfamily of orphan GPCRs as a new class of signaling modulators, Faseb. J., 27 Patel, 2015, Expression and functional role of orphan receptor GPR158 in prostate cancer growth and progression, PLoS One, 10, 10.1371/journal.pone.0117758 Patocka, 2014, Serotonin signaling in Schistosoma mansoni: a serotonin-activated G protein-coupled receptor controls parasite movement, PLoS Pathog., 10, 10.1371/journal.ppat.1003878 Pearson, 2013, An introduction to sequence similarity (“homology”) searching, Curr. Protoc. Bioinformatics, 10.1002/0471250953.bi0301s42 Petersen, 2008, Smed-betacatenin-1 is required for anterioposterior blastema polarity in planarian regeneration, Science, 319, 327, 10.1126/science.1149943 Ribeiro, 2013, Neurotransmitter transporters in schistosomes: structure, function and prospects for drug discovery, Parasitol. Int., 62, 629, 10.1016/j.parint.2013.06.003 Ribeiro, 1983, The occurrence and synthesis of octopamine and catecholamines in the cestode Hymenolepis diminuta, Mol. Biochem. Parasitol., 7, 53, 10.1016/0166-6851(83)90116-0 Ribeiro, 2005, Classical transmitters and their receptors in flatworms, Parasitology, 131, S19, 10.1017/S0031182005008565 Rinaldi, 2008, Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica, PLoS Neglected Trop. Dis., 2, 10.1371/journal.pntd.0000260 Roberts, 2011, Improving RNA-Seq expression estimates by correcting for fragment bias, Genome Biol., 12, R22, 10.1186/gb-2011-12-3-r22 Saberi, 2016, GPCRs direct germline development and somatic gonad function in planarians, PLoS Biol., 14, 10.1371/journal.pbio.1002457 Saeger, 2001, Latrophilin-like receptor from the parasitic nematode Haemonchus contortus as a target for the anthelmintic depsipeptide PF1022A, Faseb. J., 15, 1332, 10.1096/fj.00-0664fje Santos, 2017, A comprehensive map of molecular drug targets, Nat. Rev. Drug Discov., 16, 19, 10.1038/nrd.2016.230 Sariözkan, 2011, Estimating the total cost of bovine fasciolosis in Turkey, Ann. Trop. Med. Parasitol., 105, 439, 10.1179/1364859411Y.0000000031 Sautel, 1995, Role of a hydrophobic pocket of the human Y1 neuropeptide Y receptor in ligand binding, Mol. Cell. Endocrinol., 112, 215, 10.1016/0303-7207(95)03603-5 Sautel, 1996, Neuropeptide Y and the non-peptide antagonist BIBP 3226 share an overlapping binding site at the human Y1 receptor, Mol. Pharmacol., 50, 285 Smallwood, 2007, Mutational analysis of Norrin-Frizzled4 recognition, J. Biol. Chem., 282, 4057, 10.1074/jbc.M609618200 Stockert, 2015, Advancements in therapeutically targeting orphan GPCRs, Front. Pharmacol., 6, 100, 10.3389/fphar.2015.00100 Ta, 2015, Characterization and expression analysis of Wnt5 in Schistosoma japonicum at different developmental stages, Parasitol. Res., 114, 3261, 10.1007/s00436-015-4545-5 Taman, 2009, Investigation of a dopamine receptor in Schistosoma mansoni: functional studies and immunolocalization, Mol. Biochem. Parasitol., 168, 24, 10.1016/j.molbiopara.2009.06.003 Toet, 2014, Liver fluke vaccines in ruminants: strategies, progress and future opportunities, Int. J. Parasitol., 44, 915, 10.1016/j.ijpara.2014.07.011 Trapnell, 2009, TopHat: discovering splice junctions with RNA-seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Trapnell, 2010, Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation, Nat. Biotechnol., 28, 511, 10.1038/nbt.1621 Trapnell, 2012, Differential analysis of gene regulation at transcript resolution with RNA-Seq, Nat. Biotechnol., 31, 46, 10.1038/nbt.2450 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Tsai, 2013, The genomes of four tapeworm species reveal adaptations to parasitism, Nature, 496, 57, 10.1038/nature12031 Tusnday, 1998, Principals governing amino acid composition of integral membrane proteins: application to topology prediction, J. Mol. Biol., 283, 489, 10.1006/jmbi.1998.2107 Tusnday, 2001, The HMMTOP transmembrane topology prediction server, Bioinformatics, 17, 849, 10.1093/bioinformatics/17.9.849 Vilella, 2009, EnsemblCompara GeneTrees: complete, duplication-aware pylogenetic trees in vertebrates, Genome Res., 19, 327, 10.1101/gr.073585.107 Vogel, 2013, Phylogenetic investigation of peptide hormone and growth factor receptors in five dipteran genomes, Front. Endocrinol., 4, 193, 10.3389/fendo.2013.00193 Wacker, 2013, Structural features for functional selectivity at serotonin receptors, Science, 340, 615, 10.1126/science.1232808 Wang, 2009, Molecular basis for amino acid sensing by family C G-protein-coupled receptors, Br. J. Pharmacol., 156, 869, 10.1111/j.1476-5381.2008.00078.x Wang, 2013, Structural basis for molecular recognition at serotonin receptors, Science, 340, 610, 10.1126/science.1232807 Wang, 2013, Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni, Elife, 2, 10.7554/eLife.00768 Wellendorph, 2009, Molecular basis for amino acid sensing by family C G-protein-coupled receptors., Br. J. Pharmacol, 156, 869, 10.1111/j.1476-5381.2008.00078.x Willert, 2012, Wnt proteins, Cold Spring Harb. Perspect. Biol., 4, 10.1101/cshperspect.a007864 Winkelhagen, 2012, Apparent triclabendazole-resistant human Fasciola hepatica infection, The Netherlands, Emerg. Infect. Dis., 18, 1028, 10.3201/eid1806.120302 Wolstenholme, 2011, Ion channels and receptors as targets for the control of parasitic nematodes, Int. J. Parasitol. Drugs Drug Resist, 1, 2, 10.1016/j.ijpddr.2011.09.003 Yoshida, 2012, Orphan GPCRs and methods for identifying their ligands, Methods Enzymol., 514, 33, 10.1016/B978-0-12-381272-8.00002-7 Zamanian, 2011, The repertoire of G protein-coupled receptors in the human parasite Schistosoma mansoni and the model organism Schmidtea mediterranea, BMC Genom., 12, 596, 10.1186/1471-2164-12-596 Zamanian, 2012, Novel RNAi-mediated approach to G protein-coupled receptor deorphanization: proof of principle and characterization of a planarian 5-HT receptor, PLoS One, 7, 10.1371/journal.pone.0040787