Form and Function in the Digenea

  • Alba Cortés CarbonellEmail author
  • Bernard FriedEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)


This review aims at covering the general aspects of the form and function of the major body systems in digenetic trematodes, with emphasis on the advances that have been made on this topic since the publication of the first edition of this book; this is since 2012. In particular, the advancement in the knowledge of form and function of tegumentary, sensory, neuromuscular, alimentary, respiratory, excretory, and reproductive systems is covered. Furthermore, a brief mention of the current trends in the targeting of trematode body systems for developing novel opportunities of treatment and control is provided.


Digenea Form Function Tegumentary system Sensory system Neuromuscular system Alimentary system Reproductive system Respiratory system Excretory system 


  1. Andrade LF, Mourao Mde M, Geraldo JA, Coelho FS, Silva LL, Neves RH, Volpini A, Machado-Silva JR, Araujo N, Nacif-Pimenta R, Caffrey CR, Oliveira G (2014) Regulation of Schistosoma mansoni development and reproduction by the mitogen-activated protein kinase signaling pathway. PLoS Negl Trop Dis 8:e2949PubMedPubMedCentralCrossRefGoogle Scholar
  2. Antonelli L, Quilichini Y, Foata J, Marchand B (2014) Topography and ultrastructure of the tegument of Aphallus tubarium (Rodolphi, 1819) Poche, 1926 (Digenea: Cryptogonimidae), intestinal parasite of the common Dentex dentex (Linnaeus 1758) from Valinco Gulf. Acta Parasitol 59:615–624PubMedCrossRefPubMedCentralGoogle Scholar
  3. Anuracpreeda P, Phutong S, Ngamniyom A, Panyarachun B, Sobhon P (2015) Surface topography and ultrastructural architecture of the tegument of adult Carmyerius spatiosus Brandes, 1898. Acta Trop 143:18–28PubMedCrossRefPubMedCentralGoogle Scholar
  4. Anuracpreeda P, Chawengkirttikul R, Sobhon P (2016) Surface histology, topography, and ultrastructure of the tegument of adult Orthocoelium parvipapillatum (Stiles & Goldberger, 1910). Parasitol Res 115:2757–2769PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bakhoum AJ, Quilichini Y, Justine JL, Bray RA, Ba CT, Marchand B (2015) Ultrastructural study of sperm cells in Acanthocolpidae: the case of Stephanostomum murielae and Stephanostomoides tenuis (Digenea). Peer J 3:e744PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bakhoum AJS, Miquel J, Ndiaye PI, Justine JL, Falchi A, Ba CT, Marchand B, Quilichini Y (2017) Advances in spermatological characters in the Digenea: review and proposal of spermatozoa models and their phylogenetic importance. Adv Parasitol 98:111–165PubMedCrossRefPubMedCentralGoogle Scholar
  7. Barker LR, Bueding E, Timms AR (1966) The possible role of acetylcholine in Schistosoma mansoni. Br J Pharmacol Chemother 26:656–665PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beckmann S, Buro C, Dissous C, Hirzmann J, Grevelding CG (2010a) The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathog 6:e1000769PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beckmann S, Quack T, Burmeister C, Buro C, Long T, Dissous C, Grevelding CG (2010b) Schistosoma mansoni: signal transduction processes during the development of the reproductive organs. Parasitology 137:497–520PubMedCrossRefPubMedCentralGoogle Scholar
  10. Beckmann S, Hahnel S, Cailliau K, Vanderstraete M, Browaeys E, Dissous C, Grevelding CG (2011) Characterization of the Src/Abl hybrid kinase SmTK6 of Schistosoma mansoni. J Biol Chem 286:42325–42336PubMedPubMedCentralCrossRefGoogle Scholar
  11. Beckmann S, Quack T, Dissous C, Cailliau K, Lang G, Grevelding CG (2012) Discovery of platyhelminth-specific alpha/beta-integrin families and evidence for their role in reproduction in Schistosoma mansoni. PLoS One 7:e52519PubMedPubMedCentralCrossRefGoogle Scholar
  12. Beklemishev WN (1969) Origin and development of the excretory apparatus. In: Kabata Z (ed) Principles of comparative anatomy of invertebrates, vol 2. Oliver & Boyd, Edinburgh, pp 327–352Google Scholar
  13. Bernal D, Trelis M, Montaner S, Cantalapiedra F, Galiano A, Hackenberg M, Marcilla A (2014) Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics 105:232–241PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bogitsh BJ, Carter CE, Oeltmann TN (2013) General characteristics of the Trematoda. In: Bogitsh BJ, Carter CE, Oeltmann TN (eds) Human parasitology, 4th edn. Academic Press, Waltham, pp 153–178CrossRefGoogle Scholar
  15. Born-Torrijos A, Holzer AS, Raga JA, van Beest GS, Yoneva A (2017) Description of embryonic development and ultrastructure in miracidia of Cardiocephaloides longicollis (Digenea, Strigeidae) in relation to active host finding strategy in a marine environment. J Morphol 278:1137–1148PubMedCrossRefPubMedCentralGoogle Scholar
  16. Buro C, Oliveira KC, Lu Z, Leutner S, Beckmann S, Dissous C, Cailliau K, Verjovski-Almeida S, Grevelding CG (2013) Transcriptome analyses of inhibitor-treated schistosome females provide evidence for cooperating Src-kinase and TGFbeta receptor pathways controlling mitosis and eggshell formation. PLoS Pathog 9:e1003448PubMedPubMedCentralCrossRefGoogle Scholar
  17. Buro C, Burmeister C, Quack T, Grevelding CG (2017) Identification and first characterization of SmEps8, a potential interaction partner of SmTK3 and SER transcribed in the gonads of Schistosoma mansoni. Exp Parasitol 180:55–63PubMedCrossRefPubMedCentralGoogle Scholar
  18. Carneiro VC, de Abreu da Silva IC, Torres EJ, Caby S, Lancelot J, Vanderstraete M, Furdas SD, Jung M, Pierce RJ, Fantappie MR (2014) Epigenetic changes modulate schistosome egg formation and are a novel target for reducing transmission of schistosomiasis. PLoS Pathog 10:e1004116PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chaiyadet S, Sotillo J, Smout M, Cantacessi C, Jones MK, Johnson MS, Turnbull L, Whitchurch CB, Potriquet J, Laohaviroj M, Mulvenna J, Brindley PJ, Bethony JM, Laha T, Sripa B, Loukas A (2015) Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype. J Infect Dis 212:1636–1645PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chan JD, Acharya S, Day TA, Marchant JS (2016a) Pharmacological profiling an abundantly expressed schistosome serotonergic GPCR identifies nuciferine as a potent antagonist. Int J Parasitol Drugs Drug Resist 6:364–370PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chan JD, McCorvy JD, Acharya S, Johns ME, Day TA, Roth BL, Marchant JS (2016b) A miniaturized screen of a Schistosoma mansoni serotonergic G protein-coupled receptor identifies novel classes of parasite-selective inhibitors. PLoS Pathog 12:e1005651PubMedPubMedCentralCrossRefGoogle Scholar
  22. Collins JJ III, Wendt GR, Iyer H, Newmark PA (2016) Stem cell progeny contribute to the schistosome host-parasite interface. Elife 5:e12473PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cortés A, Sotillo J, Muñoz-Antolí C, Molina-Durán J, Esteban JG, Toledo R (2017) Antibody trapping: a novel mechanism of parasite immune evasion by the trematode Echinostoma caproni. PLoS Negl Trop Dis 11:e0005773PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cwiklinski K, Dalton JP, Dufresne PJ, La Course J, Williams DJ, Hodgkinson J, Paterson S (2015a) The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biol 16:71PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cwiklinski K, de la Torre-Escudero E, Trelis M, Bernal D, Dufresne PJ, Brennan GP, O’Neill S, Tort J, Paterson S, Marcilla A, Dalton JP, Robinson MW (2015b) The extracellular vesicles of the helminth pathogen, Fasciola hepatica: biogenesis pathways and cargo molecules involved in parasite pathogenesis. Mol Cell Proteomics 14:3258–3273PubMedPubMedCentralCrossRefGoogle Scholar
  26. Da’dara AA, Bhardwaj R, Ali YB, Skelly PJ (2014) Schistosome tegumental ecto-apyrase (SmATPDase1) degrades exogenous pro-inflammatory and pro-thrombotic nucleotides. Peer J 2:e316PubMedCrossRefPubMedCentralGoogle Scholar
  27. de Abreu da Silva IC, Carneiro VC, Vicentino AR, Aguilera EA, Mohana-Borges R, Thiengo S, Fernandez MA, Fantappie MR (2016) The distinct C-terminal acidic domains of HMGB proteins are functionally relevant in Schistosoma mansoni. Int J Parasitol 46:253–262CrossRefGoogle Scholar
  28. Ding H, Liu F, Zhu L, Wu F, Liu Q, He S, Shao W, Du Y, Ren C, Shen J, Liu M (2017) Tyrosine kinase 4 is involved in the reproduction of the platyhelminth parasite Schistosoma japonicum. Parasit Vectors 10:498PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dittman JS, Kaplan JM (2008) Behavioral impact of neurotransmitter-activated G-protein-coupled receptors: muscarinic and GABAB receptors regulate Caenorhabditis elegans locomotion. J Neurosci 28:7104–7112PubMedPubMedCentralCrossRefGoogle Scholar
  30. El-Sakkary N, Chen S, Arkin MR, Caffrey CR, Ribeiro P (2018) Octopamine signaling in the metazoan pathogen Schistosoma mansoni: localization, small-molecule screening and opportunities for drug development. Dis Model Mech 11:dmm033563. Scholar
  31. El-Shehabi F, Ribeiro P (2010) Histamine signalling in Schistosoma mansoni: immunolocalisation and characterisation of a new histamine-responsive receptor (SmGPR-2). Int J Parasitol 40:1395–1406PubMedCrossRefPubMedCentralGoogle Scholar
  32. El-Shehabi F, Taman A, Moali LS, El-Sakkary N, Ribeiro P (2012) A novel G protein-coupled receptor of Schistosoma mansoni (SmGPR-3) is activated by dopamine and is widely expressed in the nervous system. PLoS Negl Trop Dis 6:e1523PubMedPubMedCentralCrossRefGoogle Scholar
  33. Eriksson KS, Johnston RN, Shaw C, Halton DW, Panula PA (1996) Widespread distribution of histamine in the nervous system of a trematode flatworm. J Comp Neurol 373:220–227PubMedCrossRefPubMedCentralGoogle Scholar
  34. Faghiri Z, Skelly PJ (2009) The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB J 23:2780–2789PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ferreira LG, Oliva G, Andricopulo AD (2015) Target-based molecular modeling strategies for schistosomiasis drug discovery. Future Med Chem 7:753–764PubMedCrossRefPubMedCentralGoogle Scholar
  36. Filippi JJ, Quilichini Y, Marchand B (2013) Topography and ultrastructure of the tegument of Deropristis inflata Molin, 1859 (Digenea: Deropristidae), a parasite of the European eel Anguilla anguilla (Osteichthyes: Anguillidae). Parasitol Res 112:517–528PubMedCrossRefPubMedCentralGoogle Scholar
  37. Fletcher HL, Hoey EM, Orr N, Trudgett A, Fairweather I, Robinson MW (2004) The occurrence and significance of triploidy in the liver fluke, Fasciola hepatica. Parasitology 128:69–72PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fried B (1997) An overview of the biology of trematodes. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC, Boca Raton, pp 1–30Google Scholar
  39. Fried B, Haseeb MA (1991) Platyhelminthes, Aspidogastrea, Monogenea, and Digenea. In: Harrison FW, Bogitsh BJ (eds) Microscopic anatomy of invertebrates, vol 3. Wiley and Liss, New York, pp 141–209Google Scholar
  40. Geadkaew A, von Bulow J, Beitz E, Tesana S, Vichasri Grams S, Grams R (2015) Bi-functionality of Opisthorchis viverrini aquaporins. Biochimie 108:149–159PubMedCrossRefPubMedCentralGoogle Scholar
  41. Gelmedin V, Morel M, Hahnel S, Cailliau K, Dissou SC, Grevelding CG (2017) Evidence for integrin - venus kinase receptor 1 alliance in the ovary of Schistosoma mansoni females controlling cell survival. PLoS Pathog 13:e1006147PubMedPubMedCentralCrossRefGoogle Scholar
  42. Greani S, Quilichini Y, Marchand B (2016) Ultrastructural study of vitellogenesis and oogenesis of Crepidostomum metoecus (Digenea, Allocreadiidae), intestinal parasite of Salmo trutta (Pisces, Teleostei). Parasite 23:47PubMedPubMedCentralCrossRefGoogle Scholar
  43. Greenberg RM (2013) ABC multidrug transporters in schistosomes and other parasitic flatworms. Parasitol Int 62:647–653PubMedPubMedCentralCrossRefGoogle Scholar
  44. Greenberg RM (2014) Ion channels and drug transporters as targets for anthelmintics. Curr Clin Microbiol Rep 1:51–60PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hahnel S, Parker-Manuel R, Dissous C, Cailliau K, Grevelding CG (2017) First characterization of SmOPG1, a novel protein involved in gonad-associated processes in Schistosoma mansoni. Mol Biochem Parasitol 213:22–25PubMedCrossRefPubMedCentralGoogle Scholar
  46. Hahnel S, Wheeler N, Lu Z, Wangwiwatsin A, McVeigh P, Maule A, Berriman M, Day T, Ribeiro P, Grevelding CG (2018) Tissue-specific transcriptome analyses provide new insights into GPCR signalling in adult Schistosoma mansoni. PLoS Pathog 14:e1006718PubMedPubMedCentralCrossRefGoogle Scholar
  47. Halton DW (2004) Microscopy and the helminth parasite. Micron 35:361–390PubMedCrossRefPubMedCentralGoogle Scholar
  48. Halton DW, Maule AG (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82:316–333CrossRefGoogle Scholar
  49. Han Q, Jia B, Hong Y, Cao X, Zhai Q, Lu K, Li H, Zhu C, Fu Z, Shi Y, Lin J (2017) Suppression of VAMP2 alters morphology of the tegument and affects glucose uptake, development and reproduction of Schistosoma japonicum. Sci Rep 7:5212PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hanna RE, Moffett D, Forster FI, Trudgett AG, Brennan GP, Fairweather I (2016) Fasciola hepatica: a light and electron microscope study of the ovary and of the development of oocytes within eggs in the uterus provides an insight into reproductive strategy. Vet Parasitol 221:93–103PubMedCrossRefPubMedCentralGoogle Scholar
  51. Hertel LA (1993) Excretion and osmoregulation in the flatworms. Trans Am Microsc Soc 112:10–17CrossRefGoogle Scholar
  52. Holmes SD, Fairweather I (1984) Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Exp Parasitol 58:194–208PubMedCrossRefPubMedCentralGoogle Scholar
  53. 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
  54. Huang Y, Li W, Lu W, Xiong C, Yang Y, Yan H, Liu KC, Cao P (2016) Cloning and in vitro characterization of a Schistosoma japonicum aquaglyceroporin that functions in osmoregulation. Sci Rep 6:35030PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kasinathan RS, Sharma LK, Cunningham C, Webb TR, Greenberg RM (2014) Inhibition or knockdown of ABC transporters enhances susceptibility of adult and juvenile schistosomes to praziquantel. PLoS Negl Trop Dis 8:e3265PubMedPubMedCentralCrossRefGoogle Scholar
  56. Keiser J, Utzinger J (2007) Advances in the discovery and development of trematocidal drugs. Expert Opin Drug Discov 2(sup1):S9–S23PubMedCrossRefPubMedCentralGoogle Scholar
  57. Kotze AC, Hunt PW, Skuce P, von Samson-Himmelstjerna G, Martin RJ, Sager H, Krücken J, Hodgkinson J, Lespine A, Jex AR, Gilleard JS, Beech RN, Wolstenholme AJ, Demeler J, Robertson AP, Charvet CL, Neveu C, Kaminsky R, Rufener L, Alberich M, Menez C, Prichard RK (2014) Int J Parasitol Drugs Drug Resist 4:164–184Google Scholar
  58. Kelley JM, Elliott TP, Beddoe T, Anderson G, Skuce P, Spithill TW (2016) Current threat of triclabendazole resistance in Fasciola hepatica. Trends Parasitol 32:458–469PubMedCrossRefPubMedCentralGoogle Scholar
  59. Krupenko DY, Dobrovolskij AA (2015) Somatic musculature in trematode hermaphroditic generation. BMC Evol Biol 15:189PubMedPubMedCentralCrossRefGoogle Scholar
  60. Krupenko D, Gonchar A (2017a) Musculature arrangement and locomotion in notocotylid cercariae (Digenea: Notocotylidae) from mud snail Ecrobia ventrosa (Montagu, 1803). Parasitol Int 66:262–271PubMedCrossRefPubMedCentralGoogle Scholar
  61. Krupenko D, Gonchar A (2017b) Ventral concavity and musculature arrangement in notocotylid maritae (Digenea: Notocotylidae). Parasitol Int 66:660–665PubMedCrossRefPubMedCentralGoogle Scholar
  62. Kumkate S, Chunchob S, Janvilisri T (2008) Expression of ATP-binding cassette multidrug transporters in the giant liver fluke Fasciola gigantica and their possible involvement in the transport of bile salts and anthelmintics. Mol Cell Biochem 317:77–84PubMedCrossRefPubMedCentralGoogle Scholar
  63. Leow CY, Willis C, Hofmann A, Jones MK (2015) Structure-function analysis of apical membrane-associated molecules of the tegument of schistosome parasites of humans: prospects for identification of novel targets for parasite control. Br J Pharmacol 172:1653–1663PubMedCrossRefPubMedCentralGoogle Scholar
  64. Levron C, Ternengo S, Marchand B (2004) Spermiogenesis and sperm ultrastructure of Poracanthium furcatum (Digenea, Opecoelidae), a parasite of Mullus surmuletus (Pisces, Teleostei). Acta Parasitol 49:190–200Google Scholar
  65. Li XH, de Castro-Borges W, Parker-Manuel S, Vance GM, Demarco R, Neves LX, Evans GJ, Wilson RA (2013) The schistosome oesophageal gland: initiator of blood processing. PLoS Negl Trop Dis 7:e2337PubMedPubMedCentralCrossRefGoogle Scholar
  66. Li XH, Stark M, Vance GM, Cao JP, Wilson RA (2014) The anterior esophageal region of Schistosoma japonicum is a secretory organ. Parasit Vectors 7:565PubMedPubMedCentralCrossRefGoogle Scholar
  67. Li XH, DeMarco R, Neves LX, James SR, Newling K, Ashton PD, Cao JP, Wilson RA, Castro-Borges W (2018) Microexon gene transcriptional profiles and evolution provide insights into blood processing by the Schistosoma japonicum esophagus. PLoS Negl Trop Dis 12:e0006235PubMedPubMedCentralCrossRefGoogle Scholar
  68. Littlewood DTJ, Bray RA, Waeschenbach A (2015) Phylogenetic patterns of diversity in cestodes and trematodes. In: Morand S, Krasnov B, Littlewood DTJ (eds) Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Cambridge University Press, Cambridge, pp 304–319CrossRefGoogle Scholar
  69. Lu Z, Sessler F, Holroyd N, Hahnel S, Quack T, Berriman M, Grevelding CG (2016) Schistosome sex matters: a deep view into gonad-specific and pairing-dependent transcriptomes reveals a complex gender interplay. Sci Rep 6:31150PubMedPubMedCentralCrossRefGoogle Scholar
  70. MacDonald K, Buxton S, Kimber MJ, Day TA, Robertson AP, Ribeiro P (2014) Functional characterization of a novel family of acetylcholine-gated chloride channels in Schistosoma mansoni. PLoS Pathog 10:e1004181PubMedPubMedCentralCrossRefGoogle Scholar
  71. MacDonald K, Kimber MJ, Day TA, Ribeiro P (2015) A constitutively active G protein-coupled acetylcholine receptor regulates motility of larval Schistosoma mansoni. Mol Biochem Parasitol 202:29–37PubMedPubMedCentralCrossRefGoogle Scholar
  72. Marcilla A, Trelis M, Cortés A, Sotillo J, Cantalapiedra F, Mínguez MT, Valero ML, Sánchez del Pino MM, Muñoz-Antolí C, Toledo R, Bernal D (2012) Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One 7:e45974PubMedPubMedCentralCrossRefGoogle Scholar
  73. Marks NJ, Maule AG (2010) Neuropeptides in helminths: occurrence and distribution. In: Geary TG, Maule AG (eds) Neuropeptide systems as targets for parasite and pest control. Springer Nature, Gewerbestrasse, pp 49–77CrossRefGoogle Scholar
  74. Matoušková P, Vokřál I, Lamka J, Skálová L (2016) The role of xenobiotic-metabolizing enzymes in anthelmintic deactivation and resistance in helminths. Trends Parasitol 32:481–491PubMedCrossRefPubMedCentralGoogle Scholar
  75. McVeigh P, Atkinson L, Marks NJ, Mousley A, Dalzell JJ, Sluder A, Hammerland L, Maule AG (2011) Parasite neuropeptide biology: seeding rational drug target selection? Int J Parasitol Drugs Drug Resist 2:76–91PubMedPubMedCentralCrossRefGoogle Scholar
  76. McVeigh P, McCammick E, McCusker P, Wells D, Hodgkinson J, Paterson S, Mousley A, Marks NJ, Maule AG (2018a) Profiling G protein-coupled receptors of Fasciola hepatica identifies orphan rhodopsins unique to phylum Platyhelminthes. Int J Parasitol Drugs Drug Resist 8:87–103PubMedPubMedCentralCrossRefGoogle Scholar
  77. McVeigh P, McCusker P, Robb E, Wells D, Gardiner E, Mousley A, Marks NJ, Maule AG (2018b) Reasons to be nervous about flukicide discovery. Trends Parasitol 34:184–196PubMedCrossRefPubMedCentralGoogle Scholar
  78. Messerli SM, Kasinathan RS, Morgan W, Spranger S, Greenberg RM (2009) Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Mol Biochem Parasitol 167:54–59PubMedPubMedCentralCrossRefGoogle Scholar
  79. Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullus barbatus (Pisces, Teleostei). Parasitol Res 86:301–310PubMedCrossRefPubMedCentralGoogle Scholar
  80. Mordvinov VA, Ershov NI, Pirozhkova DS, Pakharukov YV, Pakharukova MY (2017) ABC transporters in the liver fluke Opisthorchis felineus. Mol Biochem Parasitol 216:60–68PubMedCrossRefPubMedCentralGoogle Scholar
  81. Ndiaye PI, Quilichini Y, Marigo AM, Ba CT, Tkach VV, Marchand B (2017) Ultrastructural characteristics of the mature spermatozoon of the digenean Sclerodistomum italicum (Stossich, 1893) (Hemiuroidea, Sclerodistomidae) intestinal parasite of Hypocanthus amia (Teleostei, Carangidae). Tissue Cell 49:15–21PubMedCrossRefPubMedCentralGoogle Scholar
  82. Nollen PM (1997) Reproductive physiology and behavior of digenetic trematodes. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC, Boca Raton, pp 117–147Google Scholar
  83. Pakharukova MY, Vavilin VA, Sripa B, Laha T, Brindley PJ, Mordvinov VA (2015) Functional analysis of the unique cytochrome P450 of the liver fluke Opisthorchis felineus. PLoS Negl Trop Dis 9:e0004258PubMedPubMedCentralCrossRefGoogle Scholar
  84. Patocka N, Ribeiro P (2013) The functional role of a serotonin transporter in Schistosoma mansoni elucidated through immunolocalization and RNA interference (RNAi). Mol Biochem Parasitol 187:32–42PubMedCrossRefPubMedCentralGoogle Scholar
  85. Patocka N, Sharma N, Rashid M, Ribeiro P (2014) Serotonin signaling in Schistosoma mansoni: a serotonin-activated G protein-coupled receptor controls parasite movement. PLoS Pathog 10:e1003878PubMedPubMedCentralCrossRefGoogle Scholar
  86. Peoples RC, Fried B (2014) Form and function in the Digenea. In: Toledo R, Fried B (eds) Digenetic trematodes, 1st edn. Springer, New York, pp 3–20CrossRefGoogle Scholar
  87. Petrov A, Podvyaznaya I (2016) Muscle architecture during the course of development of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) from cercariae to metacercariae. J Helminthol 90:321–336PubMedCrossRefPubMedCentralGoogle Scholar
  88. Pinto-Almeida A, Mendes T, Armada A, Belo S, Carrilho E, Viveiros M, Afonso A (2015) The role of efflux pumps in Schistosoma mansoni praziquantel resistant phenotype. PLoS One 10:e0140147PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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
  90. Podvyaznaya IM (2006) An ultrastructural study of alimentary tract development in the cercariae of Diplostomum pseudospathaceum (Digenea: Diplostomidae). Parasitol Res 99:362–367PubMedCrossRefPubMedCentralGoogle Scholar
  91. Podvyaznaya I (2011) An ultrastructural study of alimentary tract development in the cercariae of Prosorhynchoides borealis (Digenea, Bucephalidae). Acta Zool 92:170–178CrossRefGoogle Scholar
  92. Protasio AV, van Dongen S, Collins J, Quintais L, Ribeiro DM, Sessler F, Hunt M, Rinaldi G, Collins JJ, Enright AJ, Berriman M (2017) MiR-277/4989 regulate transcriptional landscape during juvenile to adult transition in the parasitic helminth Schistosoma mansoni. PLoS Negl Trop Dis 11:e0005559PubMedPubMedCentralCrossRefGoogle Scholar
  93. Quilichini Y, Foata J, Justine JL, Bray RA, Marchand B (2010) Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diodon hystrix (Pisces, Teleostei). Parasitol Int 59:427–434PubMedCrossRefPubMedCentralGoogle Scholar
  94. Ribeiro P, El-Shehabi F, Patocka N (2005) Classical transmitters and their receptors in flatworms. Parasitology 131:S19–S40PubMedCrossRefPubMedCentralGoogle Scholar
  95. Ribeiro P, Patocka N (2013) Neurotransmitter transporters in schistosomes: structure, function and prospects for drug discovery. Parasitol Int 62:629–638PubMedCrossRefPubMedCentralGoogle Scholar
  96. Roberts LS, Janovy J Jr (2009) Trematoda: form, function, and classification of Digeneans. In: Roberts LS, Janovy J Jr (eds) Foundations of parasitology, 8th edn. McGraw-Hill, Dubuque, pp 219–245Google Scholar
  97. Sato H, Kusel JR, Thornhill J (2004) Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 128:43–52PubMedCrossRefPubMedCentralGoogle Scholar
  98. Skelly PJ, Wilson AR (2006) Making sense of the schistosome surface. Adv Parasitol 63:185–284PubMedCrossRefPubMedCentralGoogle Scholar
  99. Sotillo J, Doolan D, Loukas A (2017) Recent advances in proteomic applications for schistosomiasis research: potential clinical impact. Exp Rev Proteomics 14:171–183CrossRefGoogle Scholar
  100. Świderski Z, Montoliu I, Feliu C, Gibson DI, Miquel J (2013) A transmission electron microscopical study of the tegument of Maritrema feliui (Digenea: Microphallidae). Acta Parasitol 58:478–485PubMedCrossRefPubMedCentralGoogle Scholar
  101. Takamiya S, Fukuda K, Nakamura T, Aoki T, Sugiyama H (2010) Paragonimus westermani possesses aerobic and anaerobic mitochondria in different tissues, adapting to fluctuating oxygen tension in microaerobic habitats. Int J Parasitol 40:1651–1658PubMedCrossRefPubMedCentralGoogle Scholar
  102. Thanasuwan S, Piratae S, Brindley PJ, Loukas A, Kaewkes S, Laha T (2014) Suppression of aquaporin, a mediator of water channel control in the carcinogenic liver fluke, Opisthorchis viverrini. Parasit Vectors 7:224PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tkach VV, Achatz TJ, Hildebrand J, Greiman SE (2018) Convoluted history and confusing morphology: molecular phylogenetic analysis of dicrocoeliids reveals true systematic position of the Anenterotrematidae Yamaguti, 1958 (Platyhelminthes, Digenea). Parasitol Int 67:501–508PubMedCrossRefPubMedCentralGoogle Scholar
  104. Tolstenkov OO, Terenina NB, Serbina EA, Kreshchenko ND, Maklakova L, Jashina A (2010) The spatial relationship between the musculature and the 5-HT and FMRFamide immunoreactivities in cercaria, metacercaria and adult Opisthorchis felineus (Digenea). Acta Parasitol 55:123–132CrossRefGoogle Scholar
  105. Tran MH, Freitas TC, Cooper L, Gaze S, Gatton ML, Jones MK, Lovas E, Pearce EJ, Loukas A (2010) Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog 6:e1000840PubMedPubMedCentralCrossRefGoogle Scholar
  106. Travassos L (1944) [Revisão da familia Dicrocoeliidae Odhner, 1910] Imprensa Nacional (in Portuguese)Google Scholar
  107. Travassos L (1955) Sôbre dois novos Dicrocoeliidae de Chiroptera. An Acad Bras Cienc 27:561–565. (in Portuguese)Google Scholar
  108. Vale N, Gouveia MJ, Rinaldi G, Brindley PJ, Gärtner F, Correia da Costa JM (2017) Praziquantel for schistosomiasis: single-drug metabolism revisited, mode of action, and resistance. Antimicrob Agents Chemother 61:e02582–16Google Scholar
  109. van Herwerden L, Blair D, Agatsuma T (1999) Genetic diversity in parthenogenetic triploid Paragonimus westermani. Int J Parasitol 29:1477–1482PubMedCrossRefPubMedCentralGoogle Scholar
  110. Vanderstraete M, Gouignard N, Cailliau K, Morel M, Hahnel S, Leutner S, Beckmann S, Grevelding CG, Dissous C (2014) Venus kinase receptors control reproduction in the platyhelminth parasite Schistosoma mansoni. PLoS Pathog 10:e1004138PubMedPubMedCentralCrossRefGoogle Scholar
  111. Vicogne J, Pin JP, Lardans V, Capron M, Noel C, Dissous C (2003) An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Mol Biochem Parasitol 126:51–62PubMedCrossRefPubMedCentralGoogle Scholar
  112. Whitfield PJ, Evans NA (1983) Parthenogenesis and asexual multiplication among parasitic platyhelminths. Parasitology 86:121–160PubMedCrossRefPubMedCentralGoogle Scholar
  113. Wilkinson R, Law CJ, Hoey EM, Fairweather I, Brennan GP, Trudgett A (2012) An amino acid substitution in Fasciola hepatica P-glycoprotein from triclabendazole-resistant and triclabendazole-susceptible populations. Mol Biochem Parasitol 186:69–72PubMedCrossRefPubMedCentralGoogle Scholar
  114. Wilson RA, Li XH, MacDonald S, Neves LX, Vitoriano-Souza J, Leite LC, Farias LP, James S, Ashton PD, DeMarco R, Castro-Borges W (2015) The schistosome esophagus is a 'hotspot' for microexon and lysosomal hydrolase gene expression: implications for blood processing. PLoS Negl Trop Dis 9:e0004272PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wu C, Hou N, Piao X, Liu S, Cai P, Xiao Y, Chen Q (2015) Non-immune immunoglobulins shield Schistosoma japonicum from host immunorecognition. Sci Rep 5:13434PubMedPubMedCentralCrossRefGoogle Scholar
  116. Xiong Y, Zhang M, Hong Y, Wei M, Ai D, Meng P, Han Y, Fu Z, Shi Y, Yang J, Lin J (2013) Characterization analysis of Schistosoma japonicum plasma membrane repair relative gene myoferlin. PLoS One 8:e66396PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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, The 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
  118. Zhu L, Zhao J, Wang J, Hu C, Peng J, Luo R, Zhou C, Liu J, Lin J, Jin Y, Davis RE, Cheng G (2016) MicroRNAs are involved in the regulation of ovary development in the pathogenic blood fluke Schistosoma japonicum. PLoS Pathog 12:e1005423PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Departament de Farmàcia, Tecnologia Farmacèutica i Parasitologia, Facultat de FarmàciaUniversitat de ValènciaValenciaSpain
  2. 2.Department of BiologyLafayette CollegeEastonUSA

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