Advertisement

Trematode Genomics and Proteomics

  • Javier SotilloEmail author
  • Mark S. Pearson
  • Alex Loukas
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)

Abstract

Trematode infections are among the most neglected tropical diseases despite their worldwide distribution and extraordinary ability to parasitise many different host species and host tissues. Furthermore, these parasites are of great socioeconomic, medical, veterinary and agricultural importance. During the last 10 years, there have been increasing efforts to overcome the lack of information on different “omic” resources such as proteomics and genomics. Herein, we focus on the recent advances in genomics and proteomics from trematodes of human importance, including liver, blood, intestinal and lung flukes. We also provide information on the latest technologies applied to study the biology of trematodes as well as on the resources available for the study of the molecular aspects of this group of helminths.

Keywords

Digenea Trematode infection Genomics Proteomics Host–parasite relationships Pathogenicity Diagnosis Treatment Control 

Notes

Acknowledgements

This work was supported by a programme grant from the National Health and Medical Research Council (NHMRC) [programme grant number 1037304] and a Senior Principal Research fellowship from NHMRC to AL (1117504). The funders had no role in study design, decision to publish or preparation of the manuscript.

References

  1. Arias M, Lomba C, Dacal V, Vázquez L, Pedreira J, Francisco I, Piñeiro P, Cazapal-Monteiro C, Suárez JL, Díez-Baños P, Morrondo P, Sánchez-Andrade R, Paz-Silva A (2011) Prevalence of mixed trematode infections in an abattoir receiving cattle from northern Portugal and north-west Spain. Vet Rec 168:408PubMedCrossRefPubMedCentralGoogle Scholar
  2. Arunsan P, Ittiprasert W, Smout MJ, Cochran CJ, Mann VH, Chaiyadet S, Karinshak SE, Sripa B, Young ND, Sotillo J, Loukas A, Brindley PJ, Laha T (2018) Programmed mutation of liver fluke granulin using CRISPR/Cas9 attenuates virulence of infection-induced hepatobiliary morbidity. BioRxiv. https://doi.org/10.7554/eLife.41463
  3. Aurrecoechea C, Barreto A, Basenko EY, Brestelli J, Brunk BP, Cade S, Crouch K, Doherty R, Falke D, Fischer S, Gajria B, Harb OS, Heiges M, Hertz-Fowler C, Hu S, Iodice J, Kissinger JC, Lawrence C, Li W, Pinney DF, Pulman JA, Roos DS, Shanmugasundram A, Silva-Franco F, Steinbiss S, Stoeckert JCJ, Spruill D, Wang H, Warrenfeltz S, Zheng J (2017) EuPathDB: the eukaryotic pathogen genomics database resource. Nucleic Acids Res 45:D581–D591PubMedCrossRefPubMedCentralGoogle Scholar
  4. Banford S, Drysdale O, Hoey EM, Trudgett A, Timson DJ (2013) FhCaBP3: a Fasciola hepatica calcium binding protein with EF-hand and dynein light chain domains. Biochimie 95:751–758PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bansal PS, Smout MJ, Wilson D, Cobos-Caceres C, Dastpeyman M, Sotillo J, Seifert J, Brindley PJ, Loukas A, Daly N (2017) Development of a potent wound healing agent based on the liver fluke granulin structural fold. J Med Chem 60:4258–4266PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bargues MD, Vigo M, Horak P, Dvorak J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol 1:85–107CrossRefGoogle Scholar
  7. Barsoum RS (2013) Urinary schistosomiasis: review. J Adv Res 4:453–459PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bento AP, Gaulton A, Hersey A, Bellis LJ, Chambers J, Davies M, Krüger FA, Light Y, Mak L, Mcglinchey S, Nowotka M, Papadatos G, Santos R, Overington JP (2014) The ChEMBL bioactivity database: an update. Nucleic Acids Res 42:D1083–D1090PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bernal D, Carpena I, Espert AM, De La Rubia JE, Esteban JG, Toledo R, Marcilla A (2006) Identification of proteins in excretory/secretory extracts of Echinostoma friedi (Trematoda) from chronic and acute infections. Proteomics 6:2835–2843PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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, Lacerda D, Macedo CD, McVeigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352PubMedPubMedCentralCrossRefGoogle Scholar
  11. Biswal DK, Chatterjee A, Bhattacharya A, Tandon V (2014) The mitochondrial genome of Paragonimus westermani (Kerbert, 1878), the Indian isolate of the lung fluke representative of the family Paragonimidae (Trematoda). PeerJ 2:e484PubMedPubMedCentralCrossRefGoogle Scholar
  12. Blair D, Xu ZB, Agatsuma T (1999) Paragonimiasis and the genus Paragonimus. Adv Parasitol 42:113–222PubMedCrossRefPubMedCentralGoogle Scholar
  13. Blair D, Nawa Y, Mitreva M, Doanh PN (2016) Gene diversity and genetic variation in lung flukes (genus Paragonimus). Trans R Soc Trop Med Hyg 110:6–12PubMedCrossRefPubMedCentralGoogle Scholar
  14. Braschi S, Wilson RA (2006) Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 5:347–356PubMedCrossRefPubMedCentralGoogle Scholar
  15. Braschi S, Borges WC, Wilson RA (2006a) Proteomic analysis of the schistosome tegument and its surface membranes. Mem Inst Oswaldo Cruz 101:205–212PubMedCrossRefPubMedCentralGoogle Scholar
  16. Braschi S, Curwen RS, Ashton PD, Verjovski-Almeida S, Wilson A (2006b) The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6:1471–1482PubMedCrossRefPubMedCentralGoogle Scholar
  17. Brindley PJ, Loukas A (2017) Helminth infection-induced malignancy. PLoS Pathog 13:e1006393PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brindley PJ, Mitreva M, Ghedin E, Lustigman S (2009) Helminth genomics: the implications for human health. PLoS Negl Trop Dis 3:e538PubMedPubMedCentralCrossRefGoogle Scholar
  19. Brindley PJ, Costa JMCD, Sripa B (2015) Why does infection with some helminths cause cancer? Trends Cancer 1:174–182PubMedPubMedCentralCrossRefGoogle Scholar
  20. Burke ML, Jones MK, Gobert GN, Li YS, Ellis MK, McManus DP (2009) Immunopathogenesis of human schistosomiasis. Parasite Immunol 31:163–176PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cancela M, Ruétalo N, Dell’oca N, Da Silva E, Smircich P, Rinaldi G, Roche L, Carmona C, Alvarez-Valín F, Zaha A (2010) Survey of transcripts expressed by the invasive juvenile stage of the liver fluke Fasciola hepatica. BMC Genomics 11:227PubMedPubMedCentralCrossRefGoogle Scholar
  22. Castro-Borges W, Dowle A, Curwen RS, Thomas-Oates J, Wilson RA (2011a) Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Negl Trop Dis 5:e993PubMedPubMedCentralCrossRefGoogle Scholar
  23. Castro-Borges W, Simpson DM, Dowle A, Curwen RS, Thomas-Oates J, Beynon RJ, Wilson RA (2011b) Abundance of tegument surface proteins in the human blood fluke Schistosoma mansoni determined by QconCAT proteomics. J Proteome 74:1519–1533CrossRefGoogle Scholar
  24. Chai JY (2009) Echinostomes in humans. In: Toledo R, Fried B (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 147–183CrossRefGoogle Scholar
  25. Chai JY (2013) Paragonimiasis. Handb Clin Neurol 114:283–296PubMedCrossRefPubMedCentralGoogle Scholar
  26. Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154PubMedCrossRefPubMedCentralGoogle Scholar
  27. Chai JY, Choi MH, Yu JR, Lee SH (2003) Gymnophalloides seoi: a new human intestinal trematode. Trends Parasitol 19:109–112PubMedCrossRefPubMedCentralGoogle Scholar
  28. Chaiyadet S, Smout M, Johnson M, Whitchurch C, Turnbull L, Kaewkes S, Sotillo J, Loukas A, Sripa B (2015) Excretory/secretory products of the carcinogenic liver fluke are endocytosed by human cholangiocytes and drive cell proliferation and IL6 production. Int J Parasitol 45:773–781PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chaiyadet S, Krueajampa W, Hipkaeo W, Plosan Y, Piratae S, Sotillo J, Smout M, Sripa B, Brindley PJ, Loukas A, Laha T (2017) Suppression of mRNAs encoding CD63 family tetraspanins from the carcinogenic liver fluke Opisthorchis viverrini results in distinct tegument phenotypes. Sci Rep 7:14342–14342PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chemale G, Morphew R, Moxon JV, Morassuti AL, Lacourse EJ, Barrett J, Johnston DA, Brophy PM (2006) Proteomic analysis of glutathione transferases from the liver fluke parasite, Fasciola hepatica. Proteomics 6:6263–6273PubMedCrossRefPubMedCentralGoogle Scholar
  31. Chemale G, Perally S, Lacourse EJ, Prescott MC, Jones LM, Ward D, Meaney M, Hoey E, Brennan GP, Fairweather I, Trudgett A, Brophy PM (2010) Comparative proteomic analysis of triclabendazole response in the liver fluke Fasciola hepatica. J Proteome Res 9:4940–4951PubMedCrossRefPubMedCentralGoogle Scholar
  32. Chenault C, Hoang MP (2006) An unusual cervical finding. Arch Pathol Lab Med 130:e37–e38PubMedPubMedCentralGoogle Scholar
  33. Cheng GF, Lin JJ, Feng XG, Fu ZQ, Jin YM, Yuan CX, Zhou YC, Cai YM (2005) Proteomic analysis of differentially expressed proteins between the male and female worm of Schistosoma japonicum after pairing. Proteomics 5:511–521PubMedCrossRefPubMedCentralGoogle Scholar
  34. Cho PY, Lee MJ, Kim TI, Kang SY, Hong SJ (2006) Expressed sequence tag analysis of adult Clonorchis sinensis, the Chinese liver fluke. Parasitol Res 99:602PubMedCrossRefPubMedCentralGoogle Scholar
  35. Chung E, Kim YJ, Lee MR, Cho SH, Ju JW (2018) A 21.6 kDa tegumental protein of Clonorchis sinensis induces a Th1/Th2 mixed immune response in mice. Immun Inflamm Dis 6(4):435–447PubMedPubMedCentralCrossRefGoogle Scholar
  36. Cody JJ, Ittiprasert W, Miller AN, Henein L, Mentink-Kane MM, Hsieh MH (2016) The NIH-NIAID Schistosomiasis Resource Center at the Biomedical Research Institute: molecular redux. PLoS Negl Trop Dis 10:e0005022PubMedPubMedCentralCrossRefGoogle Scholar
  37. Coghlan A, Tyagi R, Cotton JA, Holroyd N, Rosa BA, Tsai IJ, Laetsch DR, Beech RN, Day TA, Hallsworth-Pepin K, Ke HM, Kuo TH, Lee TJ, Martin J, Maizels RM, Mutowo P, Ozersky P, Parkinson J, Reid AJ, Rawlings ND, Ribeiro DM, Swapna LS, Stanley E, Taylor DW, Wheeler NJ, Zamanian M, Zhang X, Allan F, Allen JE, Asano K, Babayan SA, Bah G, Beasley H, Bennett HM, Bisset SA, Castillo E, Cook J, Cooper PJ, Cruz-Bustos T, Cuéllar C, Devaney E, Doyle SR, Eberhard ML, Emery A, Eom KS, Gilleard JS, Gordon D, Harcus Y, Harsha B, Hawdon JM, Hill DE, Hodgkinson J, Horák P, Howe KL, Huckvale T, Kalbe M, Kaur G, Kikuchi T, Koutsovoulos G, Kumar S, Leach AR, Lomax J, Makepeace B, Matthews JB, Muro A, O’Boyle NM, Olson PD, Osuna A, Partono F, Pfarr K, Rinaldi G, Foronda P, Rollinson D, Samblas MG, Sato H, Schnyder M, Scholz T, Shafie M, Tanya VN, Toledo R, Tracey A, Urban JF, Wang LC, Zarlenga D, Blaxter ML, Mitreva M, Berriman M, International Helminth Genomes (2018) Comparative genomics of the major parasitic worms. Nat Genet 51:163–174Google Scholar
  38. Colley DG, Bustinduy AL, Secor WE, King CH (2014) Human schistosomiasis. Lancet 383:2253–2264PubMedPubMedCentralCrossRefGoogle Scholar
  39. Correnti JM, Brindley PJ, Pearce EJ (2005) Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol 143:209–215PubMedCrossRefPubMedCentralGoogle Scholar
  40. Cortés A, Sotillo J, Muñoz-Antolí C, Trelis M, Esteban JG, Toledo R (2016) Definitive host influences the proteomic profile of excretory/secretory products of the trematode Echinostoma caproni. Parasit Vectors 9:185PubMedPubMedCentralCrossRefGoogle Scholar
  41. Curwen RS, Ashton PD, Johnston DA, Wilson RA (2004) The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Mol Biochem Parasitol 138:57–66PubMedCrossRefPubMedCentralGoogle Scholar
  42. Cwiklinski K, Dalton JP, Dufresne PJ, La Course J, Williams DJ, Hodgkinson J, Paterson S (2015) The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biol 16:71–71PubMedPubMedCentralCrossRefGoogle Scholar
  43. Cwiklinski K, O’neill SM, Donnelly S, Dalton JP (2016) A prospective view of animal and human Fasciolosis. Parasite Immunol 38:558–568PubMedPubMedCentralCrossRefGoogle Scholar
  44. Dalton JP, Tom TD, Strand M (1985) Fasciola hepatica: comparison of immature and mature immunoreactive glycoproteins. Parasite Immunol 7:643–657PubMedCrossRefPubMedCentralGoogle Scholar
  45. Davies DH, Liang X, Hernandez JE, Randall A, Hirst S, Mu Y, Romero KM, Nguyen TT, Kalantari-Dehaghi M, Crotty S, Baldi P, Villarreal LP, Felgner PL (2005) Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A 102:547PubMedPubMedCentralCrossRefGoogle Scholar
  46. De Assis RR, Ludolf F, Nakajima R, Jasinskas A, Oliveira GC, Felgner PL, Gaze ST, Loukas A, Loverde PT, Bethony JM, Correa-Oliveira R, Calzavara-Silva CE (2016) A next-generation proteome array for Schistosoma mansoni. Int J Parasitol 46:411–415PubMedCrossRefPubMedCentralGoogle Scholar
  47. Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvořák J, Hsieh I, Bahgat M, Dissous C, McKerrow JH (2006) A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem 281:39316–39329PubMedCrossRefPubMedCentralGoogle Scholar
  48. Ditrich O, Kopacek P, Giboda M, Gutvirth J, Scholz T (1991) Serological differentiation of human small fluke infections using Opisthorchis viverrini and Haplorchis taichui antigens. Southeast Asian J Trop Med Public Health 22:S174–S178Google Scholar
  49. Doolan DL, Aguiar JC, Weiss WR, Sette A, Felgner PL, Regis DP, Quinones-Casas P, Yates JR, Blair PL, Richie TL, Hoffman SL, Carucci DJ (2003) Utilization of genomic sequence information to develop malaria vaccines. J Exp Biol 206:3789PubMedCrossRefPubMedCentralGoogle Scholar
  50. Driguez P, Doolan DL, Loukas A, Felgner PL, McManus DP (2010) Schistosomiasis vaccine discovery using immunomics. Parasit Vectors 3:4PubMedPubMedCentralCrossRefGoogle Scholar
  51. Driguez P, Mcwilliam HE, Gaze S, Piedrafita D, Pearson MS, Nakajima R, Duke M, Trieu A, Doolan DL, Cardoso FC, Jasinskas A, Gobert GN, Felgner PL, Loukas A, Meeusen E, Mcmanus DP (2015) Specific humoral response of hosts with variable schistosomiasis susceptibility. Immunol Cell Biol 94:52–65PubMedCrossRefPubMedCentralGoogle Scholar
  52. Driguez P, Li Y, Gaze S, Pearson MS, Nakajima R, Trieu A, Doolan DL, Felgner PL, Hou X, Cardoso FC, Jasinskas A, Gobert GN, Loukas A, McManus DP (2016) Antibody signatures reflect different disease pathologies in patients with schistosomiasis due to Schistosoma japonicum. J Infect Dis 213:122–130PubMedCrossRefPubMedCentralGoogle Scholar
  53. Franco GR, Adams MD, Soares MB, Simpson AJG, Venter JC, Pena SDJ (1995) Identification of new Schistosoma mansoni genes by the EST strategy using a directional cDNA library. Gene 152:141–147PubMedCrossRefPubMedCentralGoogle Scholar
  54. Fürst T, Keiser J, Utzinger J (2012) Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12:210–221PubMedCrossRefPubMedCentralGoogle Scholar
  55. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DMA, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498PubMedCrossRefPubMedCentralGoogle Scholar
  56. Garg G, Bernal D, Trelis M, Forment J, Ortiz J, Valero ML, Pedrola L, Martinez-Blanch J, Esteban JG, Ranganathan S, Toledo R, Marcilla A (2013) The transcriptome of Echinostoma caproni adults: further characterization of the secretome and identification of new potential drug targets. J Proteome 89:202–214CrossRefGoogle Scholar
  57. Gaze S, Driguez P, Pearson MS, Mendes T, Doolan DL, Trieu A, McManus DP, Gobert GN, Periago MV, Correa-Oliveira R, Cardoso FC, Oliveira G, Nakajima R, Jasinskas A, Hung C, Liang L, Pablo J, Bethony JM, Felgner PL, Loukas A (2014) An immunomics approach to schistosome antigen discovery: antibody signatures of naturally resistant and chronically infected individuals from endemic areas. PLoS Pathog 10:e1004033PubMedPubMedCentralCrossRefGoogle Scholar
  58. Gouveia MJ, Pakharukova MY, Laha T, Sripa B, Maksimova GA, Rinaldi G, Brindley PJ, Mordvinov VA, Amaro T, Santos LL, Costa JMCD, Vale N (2017) Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model. Carcinogenesis 38:929–937PubMedPubMedCentralCrossRefGoogle Scholar
  59. Guillou F, Roger E, Moné Y, Rognon A, Grunau C, Théron A, Mitta G, Coustau C, Gourbal BEF (2007) Excretory–secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol 155:45–56PubMedCrossRefPubMedCentralGoogle Scholar
  60. Han ET, Yang HJ, Park YJ, Park JH, Chai JY (2014) Metagonimus yokogawai: a 100-kDa somatic antigen commonly reacting with other trematodes. Korean J Parasitol 52:201–204PubMedPubMedCentralCrossRefGoogle Scholar
  61. Henry J Kaiser Family Foundation (2018) The U.S government and global neglected tropical disease efforts. https://www.kff.org/global-health-policy/fact-sheet/the-u-s-government-and-global-neglected-tropical-diseases/. Accessed 22 Oct 2018
  62. Higón M, Monteagudo C, Fried B, Esteban JG, Toledo R, Marcilla A (2008) Molecular cloning and characterization of Echinostoma caproni heat shock protein-70 and differential expression in the parasite derived from low- and high-compatible hosts. Parasitology 135:1469–1477PubMedCrossRefPubMedCentralGoogle Scholar
  63. Hillyer GV (2005) Fasciola antigens as vaccines against fascioliasis and schistosomiasis. J Helminthol 79:241–247PubMedCrossRefPubMedCentralGoogle Scholar
  64. Holroyd N, Sanchez-Flores A (2012) Producing parasitic helminth reference and draft genomes at the Wellcome Trust Sanger Institute. Parasite Immunol 34:100–107PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hong Y, Peng J, Jiang W, Fu Z, Liu J, Shi Y, Li X, Lin J (2011) Proteomic analysis of Schistosoma japonicum schistosomulum proteins that are differentially expressed among hosts differing in their susceptibility to the infection. Mol Cell Proteomics 10:M110.006098PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hong Y, Sun A, Zhang M, Gao F, Han Y, Fu Z, Shi Y, Lin J (2012) Proteomics analysis of differentially expressed proteins in schistosomula and adult worms of Schistosoma japonicum. Acta Trop 126:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  67. Howe KL, Bolt BJ, Shafie M, Kersey P, Berriman M (2017) WormBase ParaSite—a comprehensive resource for helminth genomics. Mol Biochem Parasitol 215:2–10PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hu W, Yan Q, Shen DK, Liu F, Zhu ZD, Song HD, Xu XR, Wang ZJ, Rong YP, Zeng LC, Wu J, Zhang X, Wang JJ, Xu XN, Wang SY, Fu G, Zhang XL, Wang ZQ, Brindley PJ, McManus DP, Xue CL, Feng Z, Chen Z, Han ZG (2003) Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 35:139PubMedCrossRefPubMedCentralGoogle Scholar
  69. Huang Y, Zhou Z, Hu X, Wei Q, Xu J, Wu Z, Yu X (2007) A novel tegumental protein 31.8 kDa of Clonorchis sinensis: sequence analysis, expression, and immunolocalization. Parasitol Res 102:77–81PubMedCrossRefPubMedCentralGoogle Scholar
  70. Huang Y, Chen W, Wang X, Liu H, Chen Y, Guo L, Luo F, Sun J, Mao Q, Liang P, Xie Z, Zhou C, Tian Y, Lv X, Huang L, Zhou J, Hu Y, Li R, Zhang F, Lei H, Li W, Hu X, Liang C, Xu J, Li X, Yu X (2013) The Carcinogenic liver fluke, Clonorchis sinensis: new assembly, reannotation and analysis of the genome and characterization of tissue transcriptomes. PLoS One 8:e54732PubMedPubMedCentralCrossRefGoogle Scholar
  71. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 100:1–441PubMedCentralGoogle Scholar
  72. Irving DO, Howell MJ (1982) Characterization of excretory-secretory antigens of Fasciola hepatica. Parasitology 85:179–188PubMedCrossRefPubMedCentralGoogle Scholar
  73. Ittiprasert W, Mann VH, Karinshak SE, Coghlan A, Rinaldi G, Sankaranarayanan G, Chaidee A, Tanno T, Kumkhaek C, Prangtaworn P, Mentink-Kane MJ, Cochran CJ, Driguez P, Holroyd N, Tracey A, Rodpai RH, Everts B, Hokke CH, Hoffmann KF, Berriman M, Brindley PJ (2018) Programmed genome editing of the omega-1 ribonuclease of the blood fluke, Schistosoma mansoni. bioRxiv. https://doi.org/10.7554/eLife.41337
  74. Jaja IF, Mushonga B, Green E, Muchenje V (2017) Financial loss estimation of bovine fasciolosis in slaughtered cattle in South Africa. Parasite Epidemiol Control 2:27–34PubMedPubMedCentralCrossRefGoogle Scholar
  75. Jefferies JR, Brophy PM, Barrett J (2000) Investigation of Fasciola hepatica sample preparation for two-dimensional electrophoresis. Electrophoresis 21:3724–3729PubMedCrossRefPubMedCentralGoogle Scholar
  76. Johnston DA (1997) The WHO/UNDP/World Bank Schistosoma genome initiative: current status. Parasitol Today 13:45–46CrossRefGoogle Scholar
  77. Ju JW, Joo HN, Lee MR, Cho SH, Cheun HI, Kim JY, Lee YH, Lee KJ, Sohn WM, Kim DM, Kim IC, Park BC, Kim TS (2009) Identification of a serodiagnostic antigen, legumain, by immunoproteomic analysis of excretory-secretory products of Clonorchis sinensis adult worms. Proteomics 9:3066–3078PubMedCrossRefPubMedCentralGoogle Scholar
  78. Kaewpitoon N, Laha T, Kaewkes S, Yongvanit P, Brindley PJ, Loukas A, Sripa B (2008) Characterization of cysteine proteases from the carcinogenic liver fluke, Opisthorchis viverrini. Parasitol Res 102:757–764PubMedCrossRefPubMedCentralGoogle Scholar
  79. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kiger L, Rashid AK, Griffon N, Haque M, Moens L, Gibson QH, Poyart C, Marden MC (1998) Trematode hemoglobins show exceptionally high oxygen affinity. Biophys J 75:990–998PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kim YJ, Yoo WG, Lee MR, Kang JM, Na BK, Cho SH, Park MY, Ju JW (2017) Molecular and structural characterization of the tegumental 20.6-kda protein in Clonorchis sinensis as a potential druggable target. Int J Mol Sci 18:557PubMedCentralCrossRefGoogle Scholar
  82. Kokova DA, Kostidis S, Morello J, Dementeva N, Perina EA, Ivanov VV, Ogorodova LM, Sazonov AE, Saltykova IV, Mayboroda OA (2017) Exploratory metabolomics study of the experimental opisthorchiasis in a laboratory animal model (golden hamster, Mesocricetus auratus). PLoS Negl Trop Dis 11:e0006044PubMedPubMedCentralCrossRefGoogle Scholar
  83. Kostadinova A, Hernious EA, Barret J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:18CrossRefGoogle Scholar
  84. Kueakhai P, Changklungmoa N, Riengrojpitak S, Chaichanasak P, Meemon K, Chaithirayanon K, Chantree P, Sansri V, Itagaki T, Sobhon P (2013) Vaccine potential of recombinant saposin-like protein 2 against Fasciolosis gigantica in mice. Vaccine 31:5518–5523PubMedCrossRefPubMedCentralGoogle Scholar
  85. Laha T, Pinlaor P, Mulvenna J, Sripa B, Sripa M, Smout MJ, Gasser RB, Brindley PJ, Loukas A (2007) Gene discovery for the carcinogenic human liver fluke, Opisthorchis viverrini. BMC Genomics 8:189PubMedPubMedCentralCrossRefGoogle Scholar
  86. Le TH, Blair D, McManus DP (2001) Complete DNA sequence and gene organization of the mitochondrial genome of the liver fluke, Fasciola hepatica L (Platyhelminthes; Trematoda). Parasitology 123:609–621CrossRefGoogle Scholar
  87. Le TH, Nguyen KT, Nguyen NTB, Doan HTT, Dung DT, Blair D (2017) The ribosomal transcription units of Haplorchis pumilio and H. taichui and the use of 28S rDNA sequences for phylogenetic identification of common heterophyids in Vietnam. Parasit Vectors 10:17PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lee SC, Chung YB, Kong Y, Kang SY, Cho SY (1993) Antigenic protein fractions of Metagonimus yokogawai reacting with patient sera. Korean J Parasitol 31:43–48PubMedCrossRefPubMedCentralGoogle Scholar
  89. Lee JS, Lee J, Park SJ, Yong TS (2003) Analysis of the genes expressed in Clonorchis sinensis adults using the expressed sequence tag approach. Parasitol Res 91:283–289PubMedCrossRefPubMedCentralGoogle Scholar
  90. Lee EG, Na BK, Bae YA, Kim SH, Je EY, Ju JW, Cho SH, Kim TS, Kang SY, Cho SY, Kong Y (2006) Identification of immunodominant excretory–secretory cysteine proteases of adult Paragonimus westermani by proteome analysis. Proteomics 6:1290–1300PubMedCrossRefPubMedCentralGoogle Scholar
  91. Lee JS, Lee J, Kim SH, Yong TS (2007) Molecular cloning and characterization of a major egg antigen in Paragonimus westermani and its use in ELISA for the immunodiagnosis of paragonimiasis. Parasitol Res 100:677–681PubMedCrossRefPubMedCentralGoogle Scholar
  92. Lewis FA, Liang Y-S, Raghavan N, Knight M (2008) The NIH-NIAID schistosomiasis resource center. PLoS Negl Trop Dis 2:e267PubMedPubMedCentralCrossRefGoogle Scholar
  93. Li BW, McNulty SN, Rosa BA, Tyagi R, Zeng QR, Gu KZ, Weil GJ, Mitreva M (2016) Conservation and diversification of the transcriptomes of adult Paragonimus westermani and P. skrjabini. Parasit Vectors 9:497PubMedPubMedCentralCrossRefGoogle Scholar
  94. Lima OE, Esteves CZ, Oliveira DN, Guerreiro TM, Melo CFOR, Catharino RR (2017) Mass spectrometry and metabolomics—a new approaches for helminth biochemical studies. In: Rodrigo L (ed) Human Helminthiasis. IntechOpen, London, pp 19–37Google Scholar
  95. Liu Q, Wei F, Liu W, Yang S, Zhang X (2008) Paragonimiasis: an important food-borne zoonosis in China. Trends Parasitol 24:318–323CrossRefGoogle Scholar
  96. Liu M, Ju C, Du XF, Shen HM, Wang JP, Li J, Zhang XM, Feng Z, Hu W (2015) Proteomic analysis on cercariae and schistosomula in reference to potential proteases involved in host invasion of Schistosoma japonicum larvae. J Proteome Res 14:4623–4634PubMedCrossRefPubMedCentralGoogle Scholar
  97. Liu ZX, Zhang Y, Liu YT, Chang QC, Su X, Fu X, Yue DM, Gao Y, Wang CR (2016) Complete mitochondrial genome of Echinostoma hortense (Digenea: Echinostomatidae). Korean J Parasitol 54:173–179PubMedPubMedCentralCrossRefGoogle Scholar
  98. Loman NJ, Pallen MJ (2015) Twenty years of bacterial genome sequencing. Nat Rev Microbiol 13:787PubMedCrossRefPubMedCentralGoogle Scholar
  99. Lotfy WM, Brant SV, Dejong RJ, Le TH, Demiaszkiewicz A, Rajapakse RPVJ, Perera VBVP, Laursen JR, Loker ES (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). Am J Trop Med Hyg 79:248–255PubMedPubMedCentralCrossRefGoogle Scholar
  100. Marcilla A, Pérez-García A, Espert A, Bernal D, Muñoz-Antolí C, Esteban JG, Toledo R (2007) Echinostoma caproni: identification of enolase in excretory/secretory products, molecular cloning, and functional expression. Exp Parasitol 117:57–64PubMedCrossRefPubMedCentralGoogle Scholar
  101. Martin J, Rosa BA, Ozersky P, Hallsworth-Pepin K, Zhang X, Bhonagiri-Palsikar V, Tyagi R, Wang Q, Choi YJ, Gao X, McNulty SN, Brindley PJ, Mitreva M (2015) Helminth.net: expansions to Nematode.net and an introduction to Trematode.net. Nucleic Acids Res 43:D698–D706PubMedCrossRefPubMedCentralGoogle Scholar
  102. Martin J, Tyagi R, Rosa BA, Mitreva M (2018) A multi-omics database for parasitic nematodes and trematodes. In: Kollmar M (ed) Eukaryotic genomic databases: methods and protocols. Springer, New York, pp 371–397CrossRefGoogle Scholar
  103. Mas-Coma S, Valero MA, Bargues MD (2009) Fasciola, Lymnaeids and Human Fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69:41–146CrossRefPubMedPubMedCentralGoogle Scholar
  104. Matchimakul P, Rinaldi G, Suttiprapa S, Mann VH, Popratiloff A, Laha T, Pimenta RN, Cochran CJ, Kaewkes S, Sripa B, Brindley PJ (2015) Apoptosis of cholangiocytes modulated by thioredoxin of carcinogenic liver fluke. Int J Biochem Cell Biol 65:72–80PubMedPubMedCentralCrossRefGoogle Scholar
  105. Mathieson W, Wilson RA (2010) A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. Int J Parasitol 40:617–628PubMedCrossRefPubMedCentralGoogle Scholar
  106. Mazeri S, Rydevik G, Handel I, Bronsvoort BMD, Sargison N (2017) Estimation of the impact of Fasciola hepatica infection on time taken for UK beef cattle to reach slaughter weight. Sci Rep 7:7319PubMedPubMedCentralCrossRefGoogle Scholar
  107. McManus DP, Dunne DW, Sacko M, Utzinger J, Vennervald BJ, Zhou XN (2018) Schistosomiasis. Nat Rev Dis Primers 4:13PubMedCrossRefPubMedCentralGoogle Scholar
  108. McNulty SN, Fischer PU, Townsend RR, Curtis KC, Weil GJ, Mitreva M (2014) Systems biology studies of adult paragonimus lung flukes facilitate the identification of immunodominant parasite antigens. PLoS Negl Trop Dis 8:e3242PubMedPubMedCentralCrossRefGoogle Scholar
  109. McNulty SN, Tort JF, Rinaldi G, Fischer K, Rosa BA, Smircich P, Fontenla S, Choi YJ, Tyagi R, Hallsworth-Pepin K, Mann VH, Kammili L, Latham PS, Dell’oca N, Dominguez F, Carmona C, Fischer PU, Brindley PJ, Mitreva M (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:e1006537PubMedPubMedCentralCrossRefGoogle Scholar
  110. McWilliam HEG, Driguez P, Piedrafita D, McManus DP, Meeusen ENT (2014) Discovery of novel Schistosoma japonicum antigens using a targeted protein microarray approach. Parasit Vectors 7:290PubMedPubMedCentralCrossRefGoogle Scholar
  111. Merrifield M, Hotez PJ, Beaumier CM, Gillespie P, Strych U, Hayward T, Bottazzi ME (2016) Advancing a vaccine to prevent human schistosomiasis. Vaccine 34:2988–2991PubMedPubMedCentralCrossRefGoogle Scholar
  112. Michelle-North MD, Irin-Dubinchik MD, Adel-Hamid MD, Salah-Elderiny MD, Raja-Sayegh MD (2003) Association between cervical schistosomiasis and cervical cancer: a report of 2 cases. J Reprod Med 48:4Google Scholar
  113. Mulvenna J, Moertel L, Jones MK, Nawaratna S, Lovas EM, Gobert GN, Colgrave M, Jones A, Loukas A, McManus DP (2010a) Exposed proteins of the Schistosoma japonicum tegument. Int J Parasitol 40:543–554PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mulvenna J, Sripa B, Brindley PJ, Gorman J, Jones MK, Colgrave ML, Jones A, Nawaratna S, Laha T, Suttiprapa S, Smout MJ, Loukas A (2010b) The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics 10:1063–1078PubMedPubMedCentralGoogle Scholar
  115. Nithikathkul C, Tesana S, Sithithaworn P, Balakanich S (2007) Early stage biliary and intrahepatic migration of Opisthorchis viverrini in the golden hamster. J Helminthol 81:39–41PubMedCrossRefPubMedCentralGoogle Scholar
  116. Pakharukova MY, Mordvinov VA (2016) The liver fluke Opisthorchis felineus: biology, epidemiology and carcinogenic potential. Trans R Soc Trop Med Hyg 110:28–36PubMedCrossRefPubMedCentralGoogle Scholar
  117. Palevich N, Britton C, Kamenetzky L, Mitreva M, De Moraes Mourão M, Bennuru S, Quack T, Scholte LLS, Tyagi R, Slatko BE (2018) Tackling hypotheticals in helminth genomes. Trends Parasitol 34:179–183PubMedCrossRefPubMedCentralGoogle Scholar
  118. Patti GJ, Yanes O, Siuzdak G (2012) Metabolomics: the apogee of the omics trilogy. Nat Rev Mol Cell Biol 13:263PubMedPubMedCentralCrossRefGoogle Scholar
  119. Pearson MS, Becker L, Driguez P, Young ND, Gaze S, Mendes T, Li XH, Doolan DL, Midzi N, Mduluza T, McManus DP, Wilson RA, Bethony JM, Nausch N, Mutapi F, Felgner PL, Loukas A (2015) Of monkeys and men: immunomic profiling of sera from humans and non-human primates resistant to schistosomiasis reveals novel potential vaccine candidates. Front Immunol 6:213PubMedPubMedCentralCrossRefGoogle Scholar
  120. Pinlaor P, Kaewpitoon N, Laha T, Sripa B, Kaewkes S, Morales ME, Mann VH, Parriott SK, Suttiprapa S, Robinson MW, To J, Dalton JP, Loukas A, Brindley PJ (2009) Cathepsin F cysteine protease of the human liver fluke, Opisthorchis viverrini. PLoS Negl Trop Dis 3:e398PubMedPubMedCentralCrossRefGoogle Scholar
  121. Piratae S, Tesana S, Jones MK, Brindley PJ, Loukas A, Lovas E, Eursitthichai V, Sripa B, Thanasuwan S, Laha T (2012) Molecular Characterization of a tetraspanin from the human liver fluke, Opisthorchis viverrini. PLoS Negl Trop Dis 6:e1939PubMedPubMedCentralCrossRefGoogle Scholar
  122. Pisciotta JM, Ponder EL, Fried B, Sullivan D (2005) Hemozoin formation in Echinostoma trivolvis rediae. Int J Parasitol 35:1037–1042PubMedCrossRefPubMedCentralGoogle Scholar
  123. Pozio E, Armignacco O, Ferri F, Gomez-Morales MA (2013) Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union. Acta Trop 126:54–62PubMedCrossRefPubMedCentralGoogle Scholar
  124. Protasio AV, Tsai IJ, Babbage A, Nichol S, Hunt M, Aslett MA, De Silva N, Velarde GS, Anderson TJC, 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 (2012) A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl Trop Dis 6:e1455PubMedPubMedCentralCrossRefGoogle Scholar
  125. Reed SL, McKerrow JH (2018) Why funding for neglected tropical diseases should be a global priority. Clin Infect Dis 67:323–326PubMedCrossRefPubMedCentralGoogle Scholar
  126. Roberts SM, MacGregor AN, Vojvodic M, Wells E, Crabtree JE, Wilson RA (1983) Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Mol Biochem Parasitol 9:105–127PubMedCrossRefPubMedCentralGoogle Scholar
  127. Robinson MW, Dalton JP, Donnelly S (2008) Helminth pathogen cathepsin proteases: it’s a family affair. Trends Biochem Sci 33:601–608PubMedCrossRefPubMedCentralGoogle Scholar
  128. Robinson MW, Menon R, Donnelly SM, Dalton JP, Ranganathan S (2009) An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica. Mol Cell Proteomics 8:1891PubMedPubMedCentralCrossRefGoogle Scholar
  129. Robinson MW, Donnelly S, Hutchinson AT, To J, Taylor NL, Norton RS, Perugini MA, Dalton JP (2011) A family of helminth molecules that modulate innate cell responses via molecular mimicry of host antimicrobial peptides. PLoS Pathog 7:e1002042PubMedPubMedCentralCrossRefGoogle Scholar
  130. Saijuntha W, Sithithaworn P, Duenngai K, Kiatsopit N, Andrews RH, Petney TN (2011) Genetic variation and relationships of four species of medically important echinostomes (Trematoda: Echinostomatidae) in South-East Asia. Infect Genet Evol 11:375–381PubMedCrossRefPubMedCentralGoogle Scholar
  131. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 74:5463PubMedCrossRefPubMedCentralGoogle Scholar
  132. Saric J, Want EJ, Duthaler U, Lewis M, Keiser J, Shockcor JP, Ross GA, Nicholson JK, Holmes E, Tavares MFM (2012) Systematic evaluation of extraction methods for multiplatform-based metabotyping: application to the Fasciola hepatica metabolome. Anal Chem 84:6963–6972PubMedPubMedCentralCrossRefGoogle Scholar
  133. Skelly PJ, Da’Dara AA, Li XH, Castro-Borges W, Wilson RA (2014) Schistosome feeding and regurgitation. PLoS Pathog 10:e1004246PubMedPubMedCentralCrossRefGoogle Scholar
  134. Smout MJ, Laha T, Mulvenna J, Sripa B, Suttiprapa S, Jones A, Brindley PJ, Loukas A (2009) A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog 5:e1000611PubMedPubMedCentralCrossRefGoogle Scholar
  135. Smout MJ, Sotillo J, Laha T, Papatpremsiri A, Rinaldi G, Pimenta RN, Chan LY, Johnson MS, Turnbull L, Whitchurch CB, Giacomin PR, Moran CS, Golledge J, Daly N, Sripa B, Mulvenna JP, Brindley PJ, Loukas A (2015) Carcinogenic Parasite secretes growth factor that accelerates wound healing and potentially promotes neoplasia. PLoS Pathog 11:e1005209PubMedPubMedCentralCrossRefGoogle Scholar
  136. Sohn WM, Chai JY, Yong TS, Eom KS, Yoon CH, Sinuon M, Socheat D, Lee SH (2011) Echinostoma revolutum infection in children, Pursat Province, Cambodia. Emerg Infect Dis 17:117–119PubMedPubMedCentralCrossRefGoogle Scholar
  137. Sotillo J, Valero L, Sánchez Del Pino MM, Fried B, Esteban JG, Marcilla A, Toledo R (2008) Identification of antigenic proteins from Echinostoma caproni (Trematoda) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunol 30:271–279PubMedCrossRefPubMedCentralGoogle Scholar
  138. Sotillo J, Valero ML, Sánchez Del Pino MM, Fried B, Esteban JG, Marcilla A, Toledo R (2010) Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitol Res 107:691–697PubMedCrossRefPubMedCentralGoogle Scholar
  139. Sotillo J, Pearson M, Becker L, Mulvenna J, Loukas A (2015) A quantitative proteomic analysis of the tegumental proteins from Schistosoma mansoni schistosomula reveals novel potential therapeutic targets. Int J Parasitol 45:505–516PubMedCrossRefPubMedCentralGoogle Scholar
  140. Sotillo J, Toledo R, Mulvenna J, Loukas A (2017) Exploiting helminth–host interactomes through big data. Trends Parasitol 33:875–888PubMedCrossRefPubMedCentralGoogle Scholar
  141. Sripa B, Kaewkes S (2000) Localisation of parasite antigens and inflammatory responses in experimental opisthorchiasis. Int J Parasitol 30:735–740PubMedCrossRefPubMedCentralGoogle Scholar
  142. Sripa B, Kaewkes S, Intapan PM, Maleewong W, Brindley PJ (2010a) Food-borne trematodiases in Southeast Asia: epidemiology, pathology, clinical manifestation and control. Adv Parasitol 72:305–350PubMedCrossRefPubMedCentralGoogle Scholar
  143. Sripa J, Laha T, To J, Brindley PJ, Sripa B, Kaewkes S, Dalton JP, Robinson MW (2010b) Secreted cysteine proteases of the carcinogenic liver fluke, Opisthorchis viverrini: regulation of cathepsin F activation by autocatalysis and trans-processing by cathepsin B. Cell Microbiol 12:781–795PubMedPubMedCentralCrossRefGoogle Scholar
  144. Sripa B, Brindley PJ, Mulvenna J, Laha T, Smout MJ, Mairiang E, Bethony JM, Loukas A (2012) The tumorigenic liver fluke Opisthorchis viverrini—multiple pathways to cancer. Trends Parasitol 28:395–407PubMedPubMedCentralCrossRefGoogle Scholar
  145. Suttiprapa S, Mulvenna J, Huong NT, Pearson MS, Brindley PJ, Laha T, Wongkham S, Kaewkes S, Sripa B, Loukas A (2009) Ov-APR-1, an aspartic protease from the carcinogenic liver fluke, Opisthorchis viverrini: functional expression, immunolocalization and subsite specificity. Int J Biochem Cell Biol 41:1148–1156PubMedCrossRefPubMedCentralGoogle Scholar
  146. Suttiprapa S, Sotillo J, Smout M, Suyapoh W, Chaiyadet S, Tripathi T, Laha T, Loukas A (2018) Opisthorchis viverrini proteome and host–parasite interactions. Adv Parasitol 102:45–72PubMedCrossRefPubMedCentralGoogle Scholar
  147. Tang ZL, Huang Y, Yu XB (2016) Current status and perspectives of Clonorchis sinensis and clonorchiasis: epidemiology, pathogenesis, omics, prevention and control. Infect Dis Poverty 5:71–71PubMedPubMedCentralCrossRefGoogle Scholar
  148. The Schistosoma japonicum Genome and Functional Analysis (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460:345–351Google Scholar
  149. Tkalcevic J, Ashman K, Meeusen E (1995) Fasciola hepatica—rapid identification of newly excysted juvenile proteins. Biochem Biophys Res Commun 213:169–174PubMedCrossRefPubMedCentralGoogle Scholar
  150. Toledo R (2009) Echinostomes in the definitive host: a model for the study of host-parasite relationships. In: Toledo R, Fried B (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 185–206CrossRefGoogle Scholar
  151. Toledo R, Espert AM, Muñoz-Antoli C, Marcilla A, Fried B, Esteban JG (2003) Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (trematoda) in experimentally infected rats: kinetics of coproantigen excretion. J Parasitol 89:1227–1231PubMedCrossRefPubMedCentralGoogle Scholar
  152. Toledo R, Espert A, Muñoz-Antoli C, Marcilla A, Fried B, Esteban JG (2004) Kinetics of Echinostoma caproni (Trematoda: Echinostomatidae) antigens in feces and serum of experimentally infected hamsters and rats. J Parasitol 90:752–758PubMedCrossRefPubMedCentralGoogle Scholar
  153. Toledo R, Esteban JG, Fried B (2009) Recent advances in the biology of Echinostomes. Adv Parasitol 69:147–204PubMedCrossRefPubMedCentralGoogle Scholar
  154. Toledo R, Bernal MD, Marcilla A (2011) Proteomics of foodborne trematodes. J Proteome 74:1485–1503CrossRefGoogle Scholar
  155. Torgerson P, Claxton J (1999) Epidemiology and control. In: Dalton JP (ed) Fasciolosis. CABI International Publishing, Wallingford, pp 113–149Google Scholar
  156. Torgerson PR, Devleesschauwer B, Praet N, Speybroeck N, Willingham AL, Kasuga F, Rokni MB, Zhou XN, Fèvre EM, Sripa B, Gargouri N, Fürst T, Budke CM, Carabin H, Kirk MD, Angulo FJ, Havelaar A, De Silva N (2015) World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Med 12:e1001920PubMedPubMedCentralCrossRefGoogle Scholar
  157. Tripathi T, Suttiprapa S, Sripa B (2017) Unusual thiol-based redox metabolism of parasitic flukes. Parasitol Int 66:390–395PubMedCrossRefPubMedCentralGoogle Scholar
  158. Tucker MS, Karunaratne LB, Lewis FA, Freitas TC, Liang YS (2013) Schistosomiasis. Curr Protoc Immunol 103:19.1.1–19.1.58CrossRefGoogle Scholar
  159. Van Balkom BW, Van Gestel RA, Brouwers JF, Krijgsveld J, Tielens AG, Heck AJ, Van Hellemond JJ (2005) Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. J Proteome Res 4:958–966PubMedCrossRefPubMedCentralGoogle Scholar
  160. Verjovski-Almeida S, Demarco R, Martins EAL, Guimarães PEM, Ojopi EPB, Paquola ACM, Piazza JP, Nishiyama MY Jr, Kitajima JP, Adamson RE, Ashton PD, Bonaldo MF, Coulson PS, Dillon GP, Farias LP, Gregorio SP, Ho PL, Leite RA, Malaquias LCC, Marques RCP, Miyasato PA, Nascimento ALTO, Ohlweiler FP, Reis EM, Ribeiro MA, Sá RG, Stukart GC, Soares MB, Gargioni C, Kawano T, Rodrigues V, Madeira AMBN, Wilson RA, Menck CFM, Setubal JC, Leite LCC, Dias-Neto E (2003) Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nat Genet 35:148PubMedCrossRefPubMedCentralGoogle Scholar
  161. Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Almazroa MA, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basáñez MG, Baxter A, Bell ML, Benjamin EJ, Bennett D, Bernabé E, Bhalla K, Bhandari B, Bikbov B, Abdulhak AB, Birbeck G, Black JA, Blencowe H, Blore D, Blyth F, Bolliger I, Bonaventure A, Boufous S, Bourne R, Boussinesq M, Braithwaite T, Brayne C, Bridgett L, Brooker S, Brooks P, Brugha TS, Bryan-Hancock C, Bucello C, Buchbinder R, Buckle G, Budke CM, Burch M, Burney P, Burstein R, Calabria B, Campbell B, Canter CE, Carabin H, Carapetis J, Carmona L, Cella C, Charlson F, Chen H, Cheng ATA, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, De Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahiya M, Dahodwala N, Damsere-Derry J, Danaei G, Davis A, De Leo D, Degenhardt L, Dellavalle R, Delossantos A, Denenberg J, Derrett S, Des Jarlais DC, Dharmaratne SD (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2163–2196PubMedPubMedCentralCrossRefGoogle Scholar
  162. Waikagul J, Thaenkham U (2014) Approaches to research on the systematics of fish-borne Trematodes. Academic, AmsterdamGoogle Scholar
  163. Wang X, Chen W, Huang Y, Sun J, Men J, Liu H, Luo F, Guo L, Lv X, Deng C, Zhou C, Fan Y, Li X, Huang L, Hu Y, Liang C, Hu X, Xu J, Yu X (2011) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol 12:R107PubMedPubMedCentralCrossRefGoogle Scholar
  164. Wang H, La Russa M, Qi LS (2016) CRISPR/Cas9 in genome editing and beyond. Annu Rev Biochem 85:227–264PubMedCrossRefPubMedCentralGoogle Scholar
  165. Wellcome Trust Sanger Institute (2014). http://www.sanger.ac.uk/science/collaboration/50hgp. Accessed 22 Oct 2018
  166. Williamson AL, Lecchi P, Turk BE, Choe Y, Hotez PJ, Mckerrow JH, Cantley LC, Sajid M, Craik CS, Loukas A (2004) A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms. J Biol Chem 279:35950–35957PubMedCrossRefPubMedCentralGoogle Scholar
  167. Wilson RA, Wright JM, De Castro-Borges W, Parker-Manuel SJ, Dowle AA, Ashton PD, Young ND, Gasser RB, Spithill TW (2011) Exploring the Fasciola hepatica tegument proteome. Int J Parasitol 41:1347–1359PubMedCrossRefPubMedCentralGoogle Scholar
  168. Won EJ, Kim SH, Kee SJ, Shin JH, Suh SP, Chai JY, Ryang DW, Shin MG (2016) Multiplex real-time pcr assay targeting eight parasites customized to the Korean population: potential use for detection in diarrheal stool samples from gastroenteritis patients. PLoS One 11:e0166957PubMedPubMedCentralCrossRefGoogle Scholar
  169. Wongkham C, Intapan PM, Maleewong W, Miwa M (2005) Evaluation of human IgG subclass antibodies in the serodiagnosis of paragonimiasis heterotremus. Asian Pac J Allergy Immunol 23:205–211Google Scholar
  170. Xu X, Zhang Y, Lin D, Zhang J, Xu J, Liu YM, Hu F, Qing X, Xia C, Pan W (2014) Serodiagnosis of Schistosoma japonicum infection: genome-wide identification of a protein marker, and assessment of its diagnostic validity in a field study in China. Lancet Infect Dis 14:489–497PubMedCrossRefPubMedCentralGoogle Scholar
  171. Yoo WG, Kim DW, Ju JW, Cho PY, Kim TI, Cho SH, Choi SH, Park HS, Kim TS, Hong SJ (2011) Developmental transcriptomic features of the carcinogenic liver fluke, Clonorchis sinensis. PLoS Negl Trop Dis 5:e1208PubMedPubMedCentralCrossRefGoogle Scholar
  172. Young ND, Campbell BE, Hall RS, Jex AR, Cantacessi C, Laha T, Sohn WM, Sripa B, Loukas A, Brindley PJ, Gasser RB (2010a) Unlocking the transcriptomes of two carcinogenic parasites, Clonorchis sinensis and Opisthorchis viverrini. PLoS Negl Trop Dis 4:e719PubMedPubMedCentralCrossRefGoogle Scholar
  173. Young ND, Hall RS, Jex AR, Cantacessi C, Gasser RB (2010b) Elucidating the transcriptome of Fasciola hepatica—a key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnol Adv 28:222–231PubMedCrossRefPubMedCentralGoogle Scholar
  174. Young ND, Jex AR, Cantacessi C, Hall RS, Campbell BE, Spithill TW, Tangkawattana S, Tangkawattana P, Laha T, Gasser RB (2011) A portrait of the transcriptome of the neglected trematode, Fasciola gigantica—biological and biotechnological implications. PLoS Negl Trop Dis 5:e1004PubMedPubMedCentralCrossRefGoogle Scholar
  175. 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 (2012) Whole-genome sequence of Schistosoma haematobium. Nat Genet 44:221PubMedPubMedCentralCrossRefGoogle Scholar
  176. Young ND, Nagarajan N, Lin SJ, Korhonen PK, Jex AR, Hall RS, Safavi-Hemami H, Kaewkong W, Bertrand D, Gao S, Seet Q, Wongkham S, Teh BT, Wongkham C, Intapan PM, Maleewong W, Yang X, Hu M, Wang Z, Hofmann A, Sternberg PW, Tan P, Wang J, Gasser RB (2014) The Opisthorchis viverrini genome provides insights into life in the bile duct. Nat Commun 5:4378PubMedPubMedCentralCrossRefGoogle Scholar
  177. Yull CS, Il KS, Yong KS (1987) Specific IgG antibody responses in experimental cat metagonimiasis. Korean J Parasitol 25:149–153CrossRefGoogle Scholar
  178. Zerlotini A, Heiges M, Wang H, Moraes RLV, Dominitini AJ, Ruiz JC, Kissinger JC, Oliveira G (2009) SchistoDB: a Schistosoma mansoni genome resource. Nucleic Acids Res 37:D579–D582PubMedCrossRefPubMedCentralGoogle Scholar
  179. Zerlotini A, Aguiar ERGR, Yu F, Xu H, Li Y, Young ND, Gasser RB, Protasio AV, Berriman M, Roos DS, Kissinger JC, Oliveira G (2013) SchistoDB: an updated genome resource for the three key schistosomes of humans. Nucleic Acids Res 41:D728–D731PubMedCrossRefPubMedCentralGoogle Scholar
  180. Zhai Q, Fu Z, Hong Y, Yu X, Han Q, Lu K, Li H, Dou X, Zhu C, Liu J, Lin J, Li G (2018) iTRAQ-based comparative proteomic analysis of Adult Schistosoma japonicum from water buffalo and yellow cattle. Front Microbiol 9:99PubMedPubMedCentralCrossRefGoogle Scholar
  181. Zhang M, Hong Y, Han Y, Han H, Peng J, Qiu C, Yang J, Lu K, Fu Z, Lin J (2013) Proteomic analysis of tegument-exposed proteins of female and male Schistosoma japonicum worms. J Proteome Res 12:5260–5270PubMedCrossRefPubMedCentralGoogle Scholar
  182. Zheng M, Hu K, Liu W, Hu X, Hu F, Huang L, Wang P, Hu Y, Huang Y, Li W, Liang C, Yin X, He Q, Yu X (2011) Proteomic analysis of excretory secretory products from Clonorchis sinensis adult worms: molecular characterization and serological reactivity of a excretory–secretory antigen-fructose-1,6-bisphosphatase. Parasitol Res 109:737–744PubMedCrossRefPubMedCentralGoogle Scholar
  183. Zheng M, Hu K, Liu W, Li H, Chen J, Yu X (2013) Proteomic analysis of different period excretory secretory products from Clonorchis sinensis adult worms: molecular characterization, immunolocalization, and serological reactivity of two excretory secretory antigens—methionine aminopeptidase 2 and acid phosphatase. Parasitol Res 112:1287–1297PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Centre for Molecular Therapeutics, Australian Institute for Tropical Health and Medicine, James Cook UniversityCairnsAustralia

Personalised recommendations