Identification of G protein-coupled receptors in Schistosoma haematobium and S. mansoni by comparative genomics

Parasites and Vectors

Volumn 7, Issue 1, 2014, Pages

  Campos, Tulio D L ^a,b   Young, Neil D ^a   Korhonen, Pasi K ^a   Hall, Ross S ^a   Mangiola, Stefano ^a   Lonie, Andrew ^a   Gasser, Robin B ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Inst Parasitol and Trop Vet Med   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; G PROTEIN COUPLED RECEPTOR; OPSIN; PEPTIDE; RHODOPSIN; ANTHELMINTIC AGENT; HELMINTH PROTEIN; INSECT PROTEIN;

ARTICLE; BIOINFORMATICS; COMPARATIVE STUDY; GENOMICS; HIDDEN MARKOV MODEL; NONHUMAN; PROTEIN ANALYSIS; PROTOZOAL GENETICS; SCHISTOSOMA; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA MANSONI; SUPPORT VECTOR MACHINE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTHELMINTICS; GENE EXPRESSION REGULATION; GENOMICS; HELMINTH PROTEINS; INSECT PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMA MANSONI;

EID: 84903304493     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-7-242     Document Type: Article

References (103)

1. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, Habbema JD, Engels D, Acta Trop 2003 86 125 139 10.1016/S0001-706X(03)00029-9 12745133
2. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, Lancet Infect Dis 2006 6 411 425 10.1016/S1473-3099(06) 70521-7 16790382
3. A wake up call for urinary schistosomiasis: reconciling research effort with public health importance. Rollinson D, Parasitology 2009 136 1593 1610 10.1017/S0031182009990552 19627633
4. Human schistosomiasis. Gryseels B, Polman K, Clerinx J, Kestens L, Lancet 2006 368 1106 1118 10.1016/S0140-6736(06)69440-3 16997665
5. Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Doenhoff MJ, Cioli D, Utzinger J, Curr Opin Infect Dis 2008 21 659 667 10.1097/QCO.0b013e328318978f 18978535
6. Interpreting low praziquantel cure rates of Schistosoma mansoni infections in Senegal. Danso-Appiah A, De Vlas SJ, Trends Parasitol 2002 18 125 129 10.1016/S1471-4922(01)02209-7 11854090
7. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, Wynn NB, Mutuku MW, Karanja DM, Colley DG, Black CL, Secor WE, Mkoji GM, Loker ES, PLoS Negl Trop Dis 2009 3 504 10.1371/journal.pntd.0000504 19688043
8. Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group. Rollinson D, Stothard JR, Southgate VR, Parasitology 2001 123 245 S260 11769287
9. Schistosoma mansoni and Biomphalaria: past history and future trends. Morgan JA, Dejong RJ, Snyder SD, Mkoji GM, Loker ES, Parasitology 2001 123 Suppl 211 228 11769285
10. The immunobiology of schistosomiasis. Pearce EJ, MacDonald AS, Nat Rev Immunol 2002 2 499 511 10.1038/nri843 12094224
11. The unacknowledged impact of chronic schistosomiasis. King CH, Dangerfield-Cha M, Chronic Illn 2008 4 65 79 10.1177/1742395307084407 18322031
12. Association between schistosomiasis and cancer. Palumbo E, Infect Dis Clin Prac 2007 15 145 148 10.1097/01.idc.0000269904.90155.ce
13. A review of human carcinogens-Part B: biological agents. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, Ghissassi FE, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V, Lancet Oncol 2009 10 321 322 10.1016/S1470-2045(09)70096-8 19350698
14. HIV target cells in Schistosoma haematobium-infected female genital mucosa. Jourdan PM, Holmen SD, Gundersen SG, Roald B, Kjetland EF, Am J Trop Med Hyg 2011 85 1060 1064 10.4269/ajtmh.2011.11-0135 22144444
15. Male-female larval interactions in Schistosoma mansoni-infected Biomphalaria glabrata. Boissier J, Mone H, Int J Parasitol 2001 31 352 358 10.1016/S0020-7519(01)00119-9 11306113
16. The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions. Jones MK, Gobert GN, Zhang L, Sunderland P, McManus DP, Bioessays 2004 26 752 765 10.1002/bies.20058 15221857
17. Functions of the tegument of schistosomes: clues from the proteome and lipidome. Van Hellemond JJ, Retra K, Brouwers JF, van Balkom BW, Yazdanbakhsh M, Shoemaker CB, Tielens AG, Int J Parasitol 2006 36 691 699 10.1016/j.ijpara. 2006.01.007 16545817
18. The cell biology of schistosomes: a window on the evolution of the early metazoa. Wilson RA, Protoplasma 2012 249 503 518 10.1007/s00709-011-0326-x 21976269
19. Schistosomes-proteomics studies for potential novel vaccines and drug targets. DeMarco R, Verjovski-Almeida S, Drug Discov Today 2009 14 472 478 10.1016/j.drudis.2009.01.011 19429506
20. A novel Schistosoma mansoni G protein-coupled receptor is responsive to histamine. Hamdan FF, Abramovitz M, Mousa A, Xie JL, Durocher Y, Hamdan FF, Abramovitz M, Mousa A, Xie JL, Durocher Y, Ribeiro P, Mol Biochem Parasitol 2002 119 75 86 10.1016/S0166-6851(01)00400-5 11755188
21. The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Braschi S, Curwen RS, Ashton PD, Verjovski-Almeida S, Wilson A, Proteomics 2006 6 1471 1482 10.1002/pmic.200500368 16447162
22. Developmental expression analysis and immunolocalization of a biogenic amine receptor in Schistosoma mansoni. El-Shehabi F, Vermeire JJ, Yoshino TP, Ribeiro P, Exp Parasitol 2009 122 17 27 10.1016/j.exppara.2009.01.001 19545530
23. A novel G protein-coupled receptor of Schistosoma mansoni (SmGPR-3) is activated by dopamine and is widely expressed in the nervous system. El-Shehabi F, Taman A, Moali LS, El-Sakkary N, Ribeiro P, PLoS Negl Trop Dis 2012 6 1523 10.1371/journal.pntd.0001523 22389736
24. Structural diversity of G protein-coupled receptors and significance for drug discovery. Lagerstrom MC, Schiöth HB, Nat Rev Drug Discov 2008 7 339 357 10.1038/nrd2518 18382464
25. The GPCR Network: a large-scale collaboration to determine human GPCR structure and function. Stevens RC, Cherezov V, Katritch V, Abagyan R, Kuhn P, Stevens RC, Cherezov V, Katritch V, Abagyan R, Kuhn P, Rosen H, Wüthrich K, Nat Rev Drug Discov 2013 12 25 34 23237917
26. GCRDb: a G-protein-coupled receptor database. Kolakowski LF Jr, Receptors Channels 1994 2 1 7 8081729
27. The GRAFS classification system of G-protein coupled receptors in comparative perspective. Schiöth HB, Fredriksson R, Gen Comp Endocrinol 2005 142 94 101 10.1016/j.ygcen.2004.12.018 15862553
28. GPCR agonists and antagonists in the clinic. Tyndall JD, Sandilya R, Med Chem 2005 1 405 421 10.2174/1573406054368675 16789897
29. Allosteric modulators of rhodopsin-like G protein-coupled receptors: opportunities in drug development. Müller CE, Schiedel AC, Baqi Y, Pharmacol Ther 2012 135 292 315 10.1016/j.pharmthera.2012.06.002 22728155
30. G protein-coupled receptors in Anopheles gambiae. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ, Science 2002 298 176 178 10.1126/science.1076196 12364795
31. The G protein-coupled receptor repertoires of human and mouse. Vassilatis DK, Hohmann JG, Zeng H, Li F, Ranchalis JE, Vassilatis DK, Hohmann JG, Zeng H, Li F, Ranchalis JE, Mortrud MT, Brown A, Rodriguez SS, Weller JR, Wright AC, Bergmann JE, Gaitanaris GA, Proc Natl Acad Sci U S A 2003 100 4903 4908 10.1073/pnas.0230374100 12679517
32. Cross genome phylogenetic analysis of human and Drosophila G protein-coupled receptors: application to functional annotation of orphan receptors. Metpally RP, Sowdhamini R, BMC Genomics 2005 6 106 10.1186/1471-2164-6-106 16091152
33. Genome wide survey of G protein-coupled receptors in Tetraodon nigroviridis. Metpally RP, Sowdhamini R, BMC Evol Biol 2005 5 41 10.1186/1471-2148-5-41 16022726
34. Characterization of the Caenorhabditis elegans G protein-coupled serotonin receptors. Carre-Pierrat M, Baillie D, Johnsen R, Hyde R, Hart A, Granger L, Segalat L, Invert Neurosci 2006 6 189 205 10.1007/s10158-006-0033-z 17082916
35. Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Bjarnadottir TK, Gloriam DE, Hellstrand SH, Kristiansson H, Fredriksson R, Schiöth HB, Genomics 2006 88 263 273 10.1016/j.ygeno.2006.04.001 16753280
36. The G protein-coupled receptor subset of the chicken genome. Lagerström MC, Hellström AR, Gloriam DE, Larsson TP, Schiöth HB, Fredriksson R, PLoS Comput Biol 2006 2 54 10.1371/journal.pcbi.0020054 16741557
37. The G protein-coupled receptor subset of the rat genome. Gloriam DE, Fredriksson R, Schiöth HB, BMC Genomics 2007 8 338 10.1186/1471-2164-8-338 17892602
38. The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis. Kamesh N, Aradhyam GK, Manoj N, BMC Evol Biol 2008 8 129 10.1186/1471-2148-8-129 18452600
39. The amphioxus (Branchiostoma floridae) genome contains a highly diversified set of G protein-coupled receptors. Nordström KJ, Fredriksson R, Schiöth HB, BMC Evol Biol 2008 8 9 10.1186/1471-2148-8-9 18199322
40. The repertoire of G-protein-coupled receptors in Xenopus tropicalis. Ji Y, Zhang Z, Hu Y, BMC Genomics 2009 10 263 10.1186/1471-2164-10-263 19508718
41. The G protein-coupled receptor subset of the dog genome is more similar to that in humans than rodents. Haitina T, Fredriksson R, Foord SM, Schiöth HB, Gloriam DE, BMC Genomics 2009 10 24 10.1186/1471-2164-10-24 19146662
42. Proteomic applications of automated GPCR classification. Davies MN, Gloriam DE, Secker A, Freitas AA, Mendao M, Davies MN, Gloriam DE, Secker A, Freitas AA, Mendao M, Timmis J, Flower DR, Proteomics 2007 7 2800 2814 10.1002/pmic.200700093 17639603
43. A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Wistrand M, Kall L, Sonnhammer EL, Protein Sci 2006 15 509 521 10.1110/ps.051745906 16452613
44. Classifying G-protein coupled receptors with support vector machines. Karchin R, Karplus K, Haussler D, Bioinformatics 2002 18 147 159 10.1093/bioinformatics/18.1.147 11836223
45. The repertoire of G protein-coupled receptors in the human parasite Schistosoma mansoni and the model organism Schmidtea mediterranea. Zamanian M, Kimber MJ, McVeigh P, Carlson SA, Maule AG, Day TA, BMC Genomics 2011 12 596 10.1186/1471-2164-12-596 22145649
46. A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. Webster BL, Southgate VR, Littlewood DT, Int J Parasitol 2006 36 947 955 10.1016/j.ijpara.2006.03.005 16730013
47. Whole-genome sequence of Schistosoma haematobium. Young ND, Jex AR, Li B, Liu S, Yang L, Xiong Z, Li Y, Cantacessi C, Hall RS, Xu X, Chen F, Wu X, Zerlotini A, Oliveira G, Hofmann A, Zhang G, Fang X, Kang Y, Campbell BE, Loukas A, Ranganathan S, Rollinson D, Rinaldi G, Brindley PJ, Yang H, Wang J, Wang J, Gasser RB, Nat Genet 2012 44 221 225 10.1038/ng.1065 22246508
48. The genome of the blood fluke Schistosoma mansoni. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, et al. Nature 2009 460 352 358 10.1038/nature08160 19606141
49. A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. Protasio AV, Tsai IJ, Babbage A, Nichol S, Hunt M, Aslett MA, De Silva N, Velarde GS, Anderson TJ, Clark RC, Davidson C, Dillon GP, Holroyd NE, LoVerde PT, Lloyd C, McQuillan J, Oliveira G, Otto TD, Parker-Manuel SJ, Quail MA, Wilson RA, Zerlotini A, Dunne DW, Berriman M, PLoS Negl Trop Dis 2012 6 1455 10.1371/journal.pntd.0001455 22253936
50. GPCRDB: information system for G protein-coupled receptors. Vroling B, Sanders M, Baakman C, Borrmann A, Verhoeven S, Klomp J, Oliveira L, de Vlieg J, Vriend G, Nucleic Acids Res 2011 39 309 319 10.1093/nar/gkq1009 21045054
51. The Pfam protein families database. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD, Nucleic Acids Res 2012 40 290 301 10.1093/nar/gkr1065 22127870
52. IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels. Harmar AJ, Hills RA, Rosser EM, Jones M, Buneman OP, Dunbar DR, Greenhill SD, Hale VA, Sharman JL, Bonner TI, Catterall WA, Davenport AP, Delagrange P, Dollery CT, Foord SM, Gutman GA, Laudet V, Neubig RR, Ohlstein EH, Olsen RW, Peters J, Pin JP, Ruffolo RR, Searls DB, Wright MW, Spedding M, Nucleic Acids Res 2009 37 680 685 10.1093/nar/gkn728 18948278
53. Cloning and expression of a complementary DNA encoding a molluscan octopamine receptor that couples to chloride channels in HEK293 cells. Gerhardt CC, Lodder HC, Vincent M, Bakker RA, Planta RJ, Vreugdenhil E, Kits KS, van Heerikhuizen H, J Biol Chem 1997 272 6201 6207 10.1074/jbc.272.10.6201 9045634
54. Molecular cloning and pharmacological characterization of a molluscan octopamine receptor. Gerhardt CC, Bakker RA, Piek GJ, Planta RJ, Vreugdenhil E, Leysen JE, van Heerikhuizen H, Mol Pharmacol 1997 51 293 300 9203635
55. Activation of a heterologously expressed octopamine receptor coupled only to adenylyl cyclase produces all the features of presynaptic facilitation in Aplysia sensory neurons. Chang DJ, Li XC, Lee YS, Kim HK, Kim US, Cho NJ, Lo XM, Weiss KR, Kandel ER, Kaang BK, Proc Natl Acad Sci U S A 2000 97 1829 1834 10.1073/pnas.97.4.1829 10677541
56. Investigation of a dopamine receptor in Schistosoma mansoni: functional studies and immunolocalization. Taman A, Ribeiro P, Mol Biochem Parasitol 2009 168 24 33 10.1016/j.molbiopara.2009.06.003 19545592
57. Localization of biogenic amines in the foregut of Aplysia californica: catecholaminergic and serotonergic innervation. Martinez-Rubio C, Serrano GE, Miller MW, J Comp Neurol 2009 514 329 342 10.1002/cne.21991 19330814
58. Histamine signalling in Schistosoma mansoni: immunolocalisation and characterisation of a new histamine-responsive receptor (SmGPR-2). El-Shehabi F, Ribeiro P, Int J Parasitol 2010 40 1395 1406 10.1016/j.ijpara.2010.04.006 20430030
59. Characterization of a novel octopamine receptor expressed in the surf clam Spisula solidissima. Blais V, Bounif N, Dube F, Gen Comp Endocrinol 2010 167 215 227 10.1016/j.ygcen.2010.03.008 20302871
60. Rapid membrane protein topology prediction. Hennerdal A, Elofsson A, Bioinformatics 2011 27 1322 1323 10.1093/bioinformatics/btr119 21493661
61. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Katoh K, Misawa K, Kuma K, Miyata T, Nucleic Acids Res 2002 30 3059 3066 10.1093/nar/gkf436 12136088
62. Accelerated profile HMM searches. Eddy SR, PLoS Comput Biol 2011 7 1002195 10.1371/journal.pcbi.1002195 22039361
63. ENSEMBL 2013. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Garcia-Giron C, Gordon L, Hourlier T, Hunt S, Juettemann T, Kahari AK, Keenan S, Komorowska M, Kulesha E, Longden I, Maurel T, McLaren WM, Muffato M, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, et al. Nucleic Acids Res 2013 41 48 55 10.1093/nar/gks1236 23203987
64. An introduction to ROC analysis. Fawcett T, Pattern Recogn Lett 2006 27 861 874 10.1016/j.patrec.2005.10.010
65. Pairwise classification and support vector machines. Kressel UH-G, Advances in Kernel Methods Cambridge, MA, USA: MIT Press, Scholkopf B, Burges CJC, Smola AJ, 1999 255 268
66. LIBSVM: A library for support vector machines. Chang CC, Lin CJ, ACM Trans Intell Syst Technol 2011 2 27
67. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MD, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F, Sigrist CJ, Zdobnov EM, Nucleic Acids Res 2001 29 37 40 10.1093/nar/29.1.37 11125043
68. High-quality protein knowledge resource: SWISS-PROT and TrEMBL. O'Donovan C, Martin MJ, Gattiker A, Gasteiger E, Bairoch A, O'Donovan C, Martin MJ, Gattiker A, Gasteiger E, Bairoch A, Apweiler R, Brief Bioinform 2002 3 275 284 10.1093/bib/3.3.275 12230036
69. The KEGG resource for deciphering the genome. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M, Nucleic Acids Res 2004 32 277 280 10.1093/nar/gkh063 14681412
70. ChEMBL: a large-scale bioactivity database for drug discovery. Gaulton A, Bellis LJ, Bento AP, Chambers J, Davies M, Gaulton A, Bellis LJ, Bento AP, Chambers J, Davies M, Hersey A, Light Y, McGlinchey S, Michalovich D, Al-Lazikani B, Overington JP, Nucleic Acids Res 2012 40 1100 1107 10.1093/nar/gkr777 21948594
71. PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Simossis VA, Heringa J, Nucleic Acids Res 2005 33 289 294 10.1093/nar/gki390 15980472
72. The PSIPRED protein structure prediction server. McGuffin LJ, Bryson K, Jones DT, Bioinformatics 2000 16 404 405 10.1093/bioinformatics/16.4.404 10869041
73. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Kall L, Krogh A, Sonnhammer EL, Nucleic Acids Res 2007 35 429 432 10.1093/nar/gkm256 17483518
74. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Edgar RC, Nucleic Acids Res 2004 32 1792 1797 10.1093/nar/gkh340 15034147
75. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP, Syst Biol 2012 61 539 542 10.1093/sysbio/sys029 22357727
76. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Whelan S, Goldman N, Mol Biol Evol 2001 18 691 699 10.1093/oxfordjournals.molbev.a003851 11319253
77. BLAT-The BLAST-like alignment tool. Kent WJ, Genome Res 2002 12 656 664 10.1101/gr.229202. Article published online before March 2002 11932250
78. BLAST+: architecture and applications. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL, BMC Bioinformatics 2009 10 421 10.1186/1471-2105-10-421 20003500
79. Automated generation of heuristics for biological sequence comparison. Slater GS, Birney E, BMC Bioinformatics 2005 6 31 10.1186/1471-2105-6-31 15713233
80. RobiNA: a user-friendly, integrated software solution for RNA-seq-based transcriptomics. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B, Nucleic Acids Res 2012 40 622 627 10.1093/nar/gks540 22684630
81. Fast and accurate short read alignment with Burrows-Wheeler transform. Li H, Durbin R, Bioinformatics 2009 25 1754 1760 10.1093/bioinformatics/btp324 19451168
82. The Sequence Alignment/Map format and SAMtools. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Bioinformatics 2009 25 2078 2079 10.1093/bioinformatics/btp352 19505943
83. Mapping and quantifying mammalian transcriptomes by RNA-seq. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, Nat Methods 2008 5 621 628 10.1038/nmeth.1226 18516045
84. Molecular signatures of G-protein-coupled receptors. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM, Nature 2013 494 185 194 10.1038/nature11896 23407534
85. Experimental challenges to targeting poorly characterized GPCRs: uncovering the therapeutic potential for free fatty acid receptors. Hudson BD, Smith NJ, Milligan G, Adv Pharmacol 2011 62 175 218 21907910
86. Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal acoelomorpha. Paps J, Baguna J, Riutort M, Mol Biol Evol 2009 26 2397 2406 10.1093/molbev/msp150 19602542
87. Neuropeptide signalling systems in flatworms. McVeigh P, Kimber MJ, Novozhilova E, Day TA, Parasitology 2005 131 Suppl 41 55 16569292
88. Discovery of multiple neuropeptide families in the phylum Platyhelminthes. McVeigh P, Mair GR, Atkinson L, Ladurner P, Zamanian M, Novozhilova E, Marks NJ, Day TA, Maule AG, Int J Parasitol 2009 39 1243 1252 10.1016/j.ijpara.2009.03.005 19361512
89. Evolution of opsins and phototransduction. Shichida Y, Matsuyama T, Philos Trans R Soc Lond B Biol Sci 2009 364 2881 2895 10.1098/rstb.2009.0051 19720651
90. The Schistosoma japonicum genome reveals features of host-parasite interplay. Schistosoma japonicum genome functional analysis consortium, Nature 2009 460 345 351 10.1038/nature08140 19606140
91. Classical transmitters and their receptors in flatworms. Ribeiro P, El-Shehabi F, Patocka N, Parasitology 2005 131 Suppl 19 40 16569290
92. Neuronal signaling in schistosomes: current status and prospects for postgenomics. Ribeiro P, Geary TG, Can J Zool 2010 88 1 22 10.1139/Z09-126
93. Biogenic amines and the control of neuromuscular signaling in schistosomes. Ribeiro P, Gupta V, El-Sakkary N, Invert Neurosci 2012 12 13 28 10.1007/s10158-012-0132-y 22526557
94. The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Gianutsos G, Bennett JL, Comp Biochem Physiol C 1977 58 157 159 10.1016/0306-4492(77)90097-1 23928
95. Schistosoma mansoni: differences in acetylcholine, dopamine, and serotonin control of circular and longitudinal parasite muscles. Pax RA, Siefker C, Bennett JL, Exp Parasitol 1984 58 314 324 10.1016/0014-4894(84)90048-1 6500002
96. The functional role of a serotonin transporter in Schistosoma mansoni elucidated through immunolocalization and RNA interference (RNAi). Patocka N, Ribeiro P, Mol Biochem Parasitol 2013 187 32 42 10.1016/j.molbiopara.2012.11.008 23246818
97. Drug discovery for schistosomiasis: hit and lead compounds identified in a library of known drugs by medium-throughput phenotypic screening. Abdulla MH, Ruelas DS, Wolff B, Snedecor J, Lim KC, Xu F, Renslo AR, Williams J, McKerrow JH, Caffrey CR, PLoS Negl Trop Dis 2009 3 478 10.1371/journal.pntd.0000478 19597541
98. New insight into praziquantel against various developmental stages of schistosomes. Wu W, Wang W, Huang YX, Parasitol Res 2011 109 1501 1507 10.1007/s00436-011-2670-3 21984370
99. RNA-seq and microarray complement each other in transcriptome profiling. Kogenaru S, Qing Y, Guo Y, Wang N, BMC Genomics 2012 13 629 10.1186/1471-2164- 13-629 23153100
100. Overcoming the challenges of membrane protein crystallography. Carpenter EP, Beis K, Cameron AD, Iwata S, Curr Opin Struct Biol 2008 18 581 586 10.1016/j.sbi.2008.07.001 18674618
101. G protein-coupled receptors: target-based in silico screening. Senderowitz H, Marantz Y, Curr Pharm Des 2009 15 4049 4068 10.2174/ 138161209789824821 20028321
102. RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs. Rinaldi G, Morales ME, Alrefaei YN, Cancela M, Castillo E, Dalton JP, Tort JF, Brindley PJ, Mol Biochem Parasitol 2009 167 118 126 10.1016/j.molbiopara.2009.05.002 19463860
103. Genetic manipulation of Schistosoma haematobium, the neglected schistosome. Rinaldi G, Okatcha TI, Popratiloff A, Ayuk MA, Suttiprapa S, Mann VH, Liang YS, Lewis FA, Loukas A, Brindley PJ, PLoS Negl Trop Dis 2011 5 1348 10.1371/journal.pntd.0001348 22022628