Secretion of extracellular vesicles during ontogeny of the tapeworm Schistocephalus solidus.
: EVs
Cestoda
ESP
TEM
novel tegumental structures
ultrastructure
Journal
Folia parasitologica
ISSN: 1803-6465
Titre abrégé: Folia Parasitol (Praha)
Pays: Czech Republic
ID NLM: 0065750
Informations de publication
Date de publication:
16 Jan 2023
16 Jan 2023
Historique:
received:
30
08
2022
accepted:
01
11
2022
entrez:
1
2
2023
pubmed:
2
2
2023
medline:
3
2
2023
Statut:
epublish
Résumé
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).
Identifiants
pubmed: 36722286
doi: 10.14411/fp.2023.003
doi:
pii:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Références
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.
pubmed: 28668323
doi: 10.1016/j.ijpara.2017.05.003
Barber I. 2013: Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends Parasitol. 29: 556-566.
pubmed: 24145060
doi: 10.1016/j.pt.2013.09.004
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.
pubmed: 19835650
doi: 10.1017/S0031182009991466
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.
pubmed: 32592809
doi: 10.1016/j.ijpara.2020.04.004
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.
pubmed: 34454597
doi: 10.1186/s13071-021-04933-w
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.
pubmed: 32674418
doi: 10.3390/biomedicines8070213
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.
pubmed: 5706745
doi: 10.1007/BF00329477
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.
pubmed: 35690629
doi: 10.1038/s41598-022-13594-3
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.
pubmed: 5652495
doi: 10.1016/0014-4894(68)90087-8
Drurey C., Maizels R.M. 2021: Helminth extracellular vesicles: interactions with the host immune system. Mol. Immunol. 137: 124-133.
pubmed: 34246032
doi: 10.1016/j.molimm.2021.06.017
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.
pubmed: 33017416
doi: 10.1371/journal.pntd.0008586
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.
pubmed: 4732029
doi: 10.1016/0020-7519(73)90110-0
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.
pubmed: 29659599
doi: 10.1371/journal.pntd.0006438
Hessvik N.P., Llorente A. 2018: Current knowledge on exosome biogenesis and release. Cell. Mol. Life Sci. 75: 193-208.
pubmed: 28733901
doi: 10.1007/s00018-017-2595-9
Hopkins C.A., Law L M., Threadgold L.T. 1978: Schistocephalus solidus: pinocytosis by the plerocercoid tegument. Exp. Parasitol. 44: 161-172.
pubmed: 658216
doi: 10.1016/0014-4894(78)90094-2
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.
doi: 10.1007/978-3-319-19944-3_2
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.
pubmed: 22024449
doi: 10.1016/j.exppara.2011.09.009
Jakobsen P.J., Wedekind C. 1998: Copepod reaction to odor stimuli influenced by cestode infection. Behav. Ecol. 9: 414-418.
doi: 10.1093/beheco/9.4.414
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.
pubmed: 26951744
doi: 10.1186/s13071-016-1419-3
Kuperman B.I. 1988: [Functional Morphology of Lower Cestodes. Ontogenetic and Evolutionary Aspects.] Nauka, Leningrad, 167 pp. (In Russian.)
Levron C., Yoneva A., Kalbe M. 2013: Spermatological characters in the diphyllobothriidean Schistocephalus solidus (Cestoda). Acta Zool. 94: 240-247.
doi: 10.1111/j.1463-6395.2011.00549.x
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.
pubmed: 31125559
doi: 10.1016/j.actatropica.2019.05.027
Lumsden R.D. 1975: Surface ultrastructure and cytochemistry of parasitic helminths. Exp. Parasitol. 37: 267-339.
pubmed: 164363
doi: 10.1016/0014-4894(75)90078-8
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.
pubmed: 4821105
doi: 10.2307/3278452
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.
pubmed: 25536932
doi: 10.3402/jev.v3.25040
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.
pubmed: 33307002
doi: 10.1016/j.ijpara.2020.09.010
McCaig M.L., Hopkins C.A. 1963: Studies on Schistocephalus solidus. II. Establishment and longevity in the definitive host. Exp. Parasitol. 13: 273-283.
pubmed: 13932021
doi: 10.1016/0014-4894(63)90080-8
McSorley H.J., Hewitson J.P., Maizels R.M. 2013: Immunomodulation by helminth parasites: defining mechanisms and mediators. Int. J. Parasitol. 43: 301-310.
pubmed: 23291463
doi: 10.1016/j.ijpara.2012.11.011
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.
pubmed: 20637299
doi: 10.1016/j.parint.2010.07.001
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.
pubmed: 34644290
doi: 10.1371/journal.pntd.0009866
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.
pubmed: 17327153
doi: 10.1016/S0091-679X(06)79004-5
Robinson M.W., Hutchinson A.T., Donnelly S., Dalton J.P. 2010: Worm secretory molecules are causing alarm. Trends Parasitol. 26: 371-372.
pubmed: 20542734
doi: 10.1016/j.pt.2010.05.004
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.
pubmed: 32531305
doi: 10.1016/j.ijpara.2020.03.011
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.
pubmed: 24036333
doi: 10.1016/j.fsi.2013.08.029
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.
pubmed: 26771494
doi: 10.1016/j.cell.2015.11.051
Threadgold L.T., Hopkins C.A. 1981: Schistocephalus solidus and Ligula intestinalis: pinocytosis by the tegument. Exp. Parasitol. 51: 444-456.
pubmed: 6164566
doi: 10.1016/0014-4894(81)90132-6
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.
pubmed: 35719328
doi: 10.3389/fcimb.2022.903602
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.
pubmed: 7707222
doi: 10.2307/3283949
Wedekind C., Strahm D., Schärer L. 1998: Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117: 373-382.
pubmed: 9820859
doi: 10.1017/S0031182098003114
Weinreich F., Kalbe M., Benesh D. P. 2014: Making the in vitro breeding of Schistocephalus solidus more flexible. Exp. Parasitol. 139: 1-5.
pubmed: 24560832
doi: 10.1016/j.exppara.2014.02.002
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.
pubmed: 34358062
doi: 10.3390/pathogens10070912
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.
pubmed: 25979354
doi: 10.3402/jev.v4.27066
Yoneva A., Scholz T., Bruňanská M., Kuchta R. 2015: Vitellogenesis of diphyllobothriidean cestodes (Platyhelminthes). C. R. Biol. 33: 169-179.
pubmed: 25641503
doi: 10.1016/j.crvi.2015.01.001
Yoneva A., Scholz T., Kuchta R. 2018: Comparative morphology of surface ultrastructure of diphyllobothriidean tapeworms (Cestoda: Diphyllobothriidea). Invertebr. Biol. 137: 38-48.
doi: 10.1111/ivb.12202