Folia Parasitologica 70:003 (2023) | DOI: 10.14411/fp.2023.003

Secretion of extracellular vesicles during ontogeny of the tapeworm Schistocephalus solidus

Hynek Mazanec ORCID...1, 2, Nikol Bušková2, Zdenko Gardian ORCID...1, 2, Roman Kuchta ORCID...1, *
1 Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic;
2 Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic

We provide the first ultrastructural evidence of the secretion of extracellular vesicles (EVs) across all parasitic stages of the tapeworm Schistocephalus solidus (Müller, 1776) (Cestoda: Diphyllobothriidea) using a laboratory life cycle model. We confirmed the presence of EV-like bodies in all stages examined, including the hexacanth, procercoids in the copepod, Macrocyclops albidus (Jurine, 1820), plerocercoids from the body cavity of the three-spined stickleback, Gasterosteus aculeatus Linnaeus, and adults cultivated in artificial medium. In addition, we provide description of novel tegumental structures potentially involved in EV biogenesis and the presence of unique elongated EVs similar to those previously described only in Fasciola hepatica Linnaeus, 1758 (Trematoda), Hymenolepis diminuta (Rudolphi, 1819) (Cestoda), and Trypanosoma brucei Plimmer et Bradford, 1899 (Kinetoplastida).

Keywords: : EVs, Cestoda, ESP, TEM, ultrastructure, novel tegumental structures

Received: August 30, 2022; Revised: October 24, 2022; Accepted: November 1, 2022; Published online: January 16, 2023  Show citation

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Mazanec, H., Bušková, N., Gardian, Z., & Kuchta, R. (2023). Secretion of extracellular vesicles during ontogeny of the tapeworm Schistocephalus solidus. Folia Parasitologica70, Article 2023.003. https://doi.org/10.14411/fp.2023.003
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References

  1. Ancarola M.E., Marcilla A., Herz M., Macchiaroli N., Pérez M., Asurmendi S., Brehm K., Poncini C., Rosenzvit M., Cucher M. 2017: Cestode parasites release extracellular vesicles with microRNAs and immunodiagnostic protein cargo. Int. J. Parasitol. 47: 675-686. Go to original source... Go to PubMed...
  2. Barber I. 2013: Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends Parasitol. 29: 556-566. Go to original source... Go to PubMed...
  3. Barber I., Scharsack J.P. 2010: The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137: 411-424. Go to original source... Go to PubMed...
  4. Bennett A.P., de la Torre-Escudero E., Robinson M.W. 2020: Helminth genome analysis reveals conservation of extracellular vesicle biogenesis pathways but divergence of RNA loading machinery between phyla. Int. J. Parasitol. 50: 655-661. Go to original source... Go to PubMed...
  5. Berger C.S., Laroche J., Maaroufi H., Martin H., Moon K.M., Landry C.R., Foster L.J., Aubin-Horth N. 2021: The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions. Parasit. Vectors 14: 436. Go to original source... Go to PubMed...
  6. Boysen A.T., Whitehead B., Stensballe A., Carnerup A., Nylander T., Nejsum P. 2020: Fluorescent labeling of helminth extracellular vesicles using an in vivo whole organism approach. Biomedicines 8: 213. Go to original source... Go to PubMed...
  7. Bråten T. 1968: An electron microscope study of the tegument and associated structures of the procercoid of Diphyllobothrium latum (L.). Z. Parasitenkd. 30: 95-103. Go to original source... Go to PubMed...
  8. Cavallero S., Bellini I., Pizzarelli A., Arcà B., D'Amelio S. 2022: A miRNAs catalogue from third-stage larvae and extracellular vesicles of Anisakis pegreffii provides new clues for host-parasite interplay. Sci. Rep. 12: 9667. Go to original source... Go to PubMed...
  9. Charles G.H., Orr T.S.C. 1968: Comparative fine structure of outer tegument of Ligula intestinalis and Schistocephalus solidus. Exp. Parasitol. 22: 137-149. Go to original source... Go to PubMed...
  10. Drurey C., Maizels R.M. 2021: Helminth extracellular vesicles: interactions with the host immune system. Mol. Immunol. 137: 124-133. Go to original source... Go to PubMed...
  11. Fratini F., Tamarozzi F., Macchia G., Bertuccini L., Mariconti M., Birago C., Iriarte A., Brunetti E., Cretu C.M., Akhan O., Siles-Lucas M., Díaz A., Casulli A. 2020: Proteomic analysis of plasma exosomes from cystic echinococcosis patients provides in vivo support for distinct immune response profiles in active vs inactive infection and suggests potential biomarkers. PLoS Negl. Trop. Dis. 14: e0008586. Go to original source... Go to PubMed...
  12. Grammeltvedt A.-F. 1973: Differentiation of the tegument and associated structures in Diphyllobothrium dendriticum Nitzsch (1824) (Cestoda: Pseudophyllidea). An electron microscopical study. Int. J. Parasitol. 3: 321-327. Go to original source... Go to PubMed...
  13. Harischandra H., Yuan W., Loghry H.J., Zamanian M., Kimber M.J. 2018: Profiling extracellular vesicle release by the filarial nematode Brugia malayi reveals sex-specific differences in cargo and a sensitivity to ivermectin. PLoS Negl. Trop. Dis. 12: e0006438. Go to original source... Go to PubMed...
  14. Hessvik N.P., Llorente A. 2018: Current knowledge on exosome biogenesis and release. Cell. Mol. Life Sci. 75: 193-208. Go to original source... Go to PubMed...
  15. Hopkins C.A., Law L M., Threadgold L.T. 1978: Schistocephalus solidus: pinocytosis by the plerocercoid tegument. Exp. Parasitol. 44: 161-172. Go to original source... Go to PubMed...
  16. Huang B.Q., Yeung E.C. 2015: Chemical and physical fixation of cells and tissues: an overview. In: E. Yeung, C. Stasolla, M. Sumner and B. Huang. (Eds.), Plant Microtechniques and Protocols. Springer, Cham, pp. 23-43. Go to original source...
  17. Jakobsen P.J., Scharsack J.P., Hammerschmidt K., Deines P., Kalbe M., Milinski M. 2012: In vitro transition of Schistocephalus solidus (Cestoda) from coracidium to procercoid and from procercoid to plerocercoid. Exp. Parasitol. 130: 267-273. Go to original source... Go to PubMed...
  18. Jakobsen P.J., Wedekind C. 1998: Copepod reaction to odor stimuli influenced by cestode infection. Behav. Ecol. 9: 414-418. Go to original source...
  19. Kalbe M., Eizaguirre C., Scharsack J.P., Jakobsen P.J. 2016: Reciprocal cross infection of sticklebacks with the diphyllobothriidean cestode Schistocephalus solidus reveals consistent population differences in parasite growth and host resistance. Parasit. Vectors 9: 130. Go to original source... Go to PubMed...
  20. Kuperman B.I. 1988: [Functional Morphology of Lower Cestodes. Ontogenetic and Evolutionary Aspects.] Nauka, Leningrad, 167 pp. (In Russian.)
  21. Levron C., Yoneva A., Kalbe M. 2013: Spermatological characters in the diphyllobothriidean Schistocephalus solidus (Cestoda). Acta Zool. 94: 240-247. Go to original source...
  22. Liang P., Mao L., Zhang S., Guo X., Liu G., Wang L., Hou J., Zheng Y., Luo X. 2019: Identification and molecular characterization of exosome-like vesicles derived from the Taenia asiatica adult worm. Acta Trop. 198: 105036. Go to original source... Go to PubMed...
  23. Lumsden R.D. 1975: Surface ultrastructure and cytochemistry of parasitic helminths. Exp. Parasitol. 37: 267-339. Go to original source... Go to PubMed...
  24. Lumsden R.D., Oaks J. A., Mueller J.F. 1974: Brush border development in the tegument of the tapeworm, Spirometra mansonoides. J. Parasitol. 60: 209-226. Go to original source... Go to PubMed...
  25. Marcilla A., Martin-Jaular L., Trelis M., de Menezes-Neto A., Osuna A., Bernal D., Fernandez-Becerra C., Almeida I.C., del Portillo, H.A. 2014: Extracellular vesicles in parasitic diseases. J. Extracell. Vesicles 3: 25040. Go to original source... Go to PubMed...
  26. Mazanec H., Koník P., Gardian Z., Kuchta R. 2021: Extracellular vesicles secreted by model tapeworm Hymenolepis diminuta: biogenesis, ultrastructure and protein composition. Int. J. Parasitol. 51: 327-332. Go to original source... Go to PubMed...
  27. McCaig M.L., Hopkins C.A. 1963: Studies on Schistocephalus solidus. II. Establishment and longevity in the definitive host. Exp. Parasitol. 13: 273-283. Go to original source... Go to PubMed...
  28. McSorley H.J., Hewitson J.P., Maizels R.M. 2013: Immunomodulation by helminth parasites: defining mechanisms and mediators. Int. J. Parasitol. 43: 301-310. Go to original source... Go to PubMed...
  29. Młocicki D., Świderski Z., Bruňanská M., Conn D.B. 2010: Functional ultrastructure of the hexacanth larvae in the bothriocephalidean cestode Eubothrium salvelini (Schrank, 1790) and its phylogenetic implications. Parasitol. Int. 59: 539-548. Go to original source... Go to PubMed...
  30. Mossallam S.F., Abou-El-Naga I.F., Abdel Bary A., Elmorsy E.A., Diab R.G. 2021: Schistosoma mansoni egg-derived extracellular vesicles: a promising vaccine candidate against murine schistosomiasis. PLoS Negl. Trop. Dis. 15: e0009866. Go to original source... Go to PubMed...
  31. Müller-Reichert T., Srayko M., Hyman A., O'Toole E.T., McDonald K. 2007: Correlative light and electron microscopy of early Caenorhabditis elegans embryos in mitosis. Methods Cell Biol. 79: 101-119. Go to original source... Go to PubMed...
  32. Robinson M.W., Hutchinson A.T., Donnelly S., Dalton J.P. 2010: Worm secretory molecules are causing alarm. Trends Parasitol. 26: 371-372. Go to original source... Go to PubMed...
  33. Sánchez-López C.M., Trelis M., Jara L., Cantalapiedra F., Marcilla A., Bernal D. 2020: Diversity of extracellular vesicles from different developmental stages of Fasciola hepatica. Int. J. Parasitol. 50: 663-669. Go to original source... Go to PubMed...
  34. Scharsack J.P., Gossens A., Franke F., Kurtz J. 2013: Excretory products of the cestode, Schistocephalus solidus, modulate in vitro responses of leukocytes from its specific host, the three-spined stickleback (Gasterosteus aculeatus). Fish Shellfish Immunol. 35: 1779-1787. Go to original source... Go to PubMed...
  35. Szempruch A.J., Sykes S.E., Kieft R., Dennison L., Becker A.C., Gartrell A., Martin W.J., Nakayasu E.S., Almeida I.C., Hajduk S.L. Harrington J.M. 2016: Extracellular vesicles from Trypanosoma brucei mediate virulence factor transfer and cause host anemia. Cell 164: 246-257. Go to original source... Go to PubMed...
  36. Threadgold L.T., Hopkins C.A. 1981: Schistocephalus solidus and Ligula intestinalis: pinocytosis by the tegument. Exp. Parasitol. 51: 444-456. Go to original source... Go to PubMed...
  37. Trelis M., Sánchez-López C.M., Sánchez-Palencia L.F., Ramírez-Toledo V., Marcilla A., Bernal D. 2022: Proteomic analysis of extracellular vesicles from Fasciola hepatica hatching eggs and juveniles in culture. Front. Cell. Infect. Microbiol. 12: 903602. Go to original source... Go to PubMed...
  38. Urdal K., Tierney J.F., Jakobsen P.J. 1995: The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. J. Parasitol. 81: 330-333. Go to original source... Go to PubMed...
  39. Wedekind C., Strahm D., Schärer L. 1998: Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117: 373-382. Go to original source... Go to PubMed...
  40. Weinreich F., Kalbe M., Benesh D. P. 2014: Making the in vitro breeding of Schistocephalus solidus more flexible. Exp. Parasitol. 139: 1-5. Go to original source... Go to PubMed...
  41. Wititkornkul B., Hulme B.J., Tomes J.J., Allen N.R., Davis C.N., Davey S.D., Cookson A.R., Phillips H.C., Hegarty J.M., Swain M.T., Brophy P.M., Wonfor R.E., Morphew R.M. 2021: Evidence of immune modulators in the secretome of the equine tapeworm Anoplocephala perfoliata. Pathogens 10: 912. Go to original source... Go to PubMed...
  42. Yáñez-Mó M., Siljander P.R., Andreu Z., Zavec A.B., Borras F.E., Buzas E.I., Casal E., Cappello F., Carvalho J., Colas E., Cordeiro-da Silva A., Fais S., Falcon-Perez J.M., Ghobrial I.M., Giebel B., Gimona M., Graner M., Gursel I., Gursel M., Heegaard N.H., Hendrix A., Kierulf P., Kokubun K., Kosanovic M., Kralj-Iglic V., Kramer-Albers E.M., Laitinen S., Lasser C., Lener T., Ligeti E., Line A., Lipps G., Llorente A., Lotvall J., Mancek-Keber M., Marcilla A., Mittelbrunn M., Nazarenko I., Nolte-'t Hoen E.N., Nyman T.A., O'Driscoll L., Olivan M., Oliveira C., Pallinger E., Del Portillo H.A., Reventos J., Rigau M., Rohde E., Sammar M., Sanchez-Madrid F., Santarem N., Schallmoser K., Ostenfeld M.S., Stoorvogel W., Stukelj R., Van der Grein S.G., Vasconcelos M.H., Wauben M.H., De Wever O. 2015: Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 4: 27066. Go to original source... Go to PubMed...
  43. Yoneva A., Scholz T., Bruňanská M., Kuchta R. 2015: Vitellogenesis of diphyllobothriidean cestodes (Platyhelminthes). C. R. Biol. 33: 169-179. Go to original source... Go to PubMed...
  44. Yoneva A., Scholz T., Kuchta R. 2018: Comparative morphology of surface ultrastructure of diphyllobothriidean tapeworms (Cestoda: Diphyllobothriidea). Invertebr. Biol. 137: 38-48. Go to original source...