Ultrastructural study of vitellogenesis of Ligula intestinalis (Diphyllobothriidea) reveals the presence of cytoplasmic-like cell death in cestodes

. 2015 ; 12 () : 35. [epub] 20151204

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid26640506

BACKGROUND: The tapeworm Ligula intestinalis (Diphyllobothriidea) is one of the most fascinating cestode parasites because it may cause parasitic castration of its second intermediate host, teleost freshwater fishes, due to inhibition of production of fish gonadotropic hormones. Large-sized (length up to 1 m) larvae called plerocercoids develop several months in the body cavity of freshwater fish and affect host behavior to facilitate transmission to the final host, a fish-eating bird. Vitellogenesis, i.e. formation of vitellocytes, is a key process in formation and nutrition of female gametes, oocytes in many flatworms, mainly parasitic Neodermata. The present study provides the first ultrastructural evidence in flatworms (Platyhelminthes) of the process that is interpreted as cytoplasmic-like cell death, i.e. a special case of programmed cell death (paraptosis) in vitellocytes of L. intestinalis. RESULTS: As molecular markers for paraptosis are not yet available, its identification was based on morphological criteria. Electron microscopy analyses revealed evident structural changes in vitellocytes associated with progressive cytoplasmatic vacuolation, swelling of the granular endoplasmic reticulum and mitochondria. In addition, the present study has shown that vitellocytes of L. intestinalis share numerous features in common with the members of other earliest evolved eucestodes. CONCLUSIONS: The present study indicates that paraptotic-like cell death may occur in parasitic flatworms (Neodermata). The presence of GER-bodies in mature vitellocytes indicates close relationship between the Diphyllobothriidea, Caryophyllidea and Spathebothriidea, which are considered as the earliest evolved groups of the Eucestoda. Beyond the general similarities, however, a number of differences exist between the morphology, chemical composition and amount of these inclusions which could be due to the variations in their embryonic development, life cycle strategies and definitive host groups.

Zobrazit více v PubMed

Dubinina MN. Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Delhi: Amerind Publishing Co. Pvt. Ltd; 1980.

Bagamian KH, Heins DC, Baker JA. Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. J Fish Biol. 2004;64:1568–76. doi: 10.1111/j.0022-1112.2004.00411.x. DOI

Cowx IG, Rollings D, Tumwebaze R. Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. J Fish Biol. 2008;73:2249–60. doi: 10.1111/j.1095-8649.2008.02058.x. DOI

Bouzid W, Štefka J, Hypša V, Lek S, Scholz T, Legal L, et al. Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae) Int J Parasitol. 2008;38:1465–79. doi: 10.1016/j.ijpara.2008.03.008. PubMed DOI

Štefka J, Hypša V, Scholz T. Interplay of host specificity and biogeography in the population structure of cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda) Mol Ecol. 2009;18:1187–1206. doi: 10.1111/j.1365-294X.2008.04074.x. PubMed DOI

Arme C, Bridges JF, Hoole D. Pathology of cestode infections in the vertebrate host. In: Arme C, Pappas PW, editors. Biology of the Eucestoda. London: Academic; 1983. pp. 499–538.

Conn DB. Atlas of invertebrate reproduction and development. 2. New York: John Wiley & Sons; 2000.

Świderski Z, Xylander WER. Vitellocytes and vitellogenesis in cestodes in relation to embryonic development egg production and life cycles. Int J Parasitol. 2000;30:805–17. doi: 10.1016/S0020-7519(00)00066-7. PubMed DOI

Fitzpatrick JM, Hirai Y, Hirai H, Hoffmann KF. Schistosome egg production is dependent upon the activities of two developmentally regulated tyrosinases. FASEB J. 2007;21:823–35. doi: 10.1096/fj.06-7314com. PubMed DOI

Yoneva A, Kuchta R, Scholz T. First study of vitellogenesis of the broad fish tapeworm Diphyllobothrium latum (Cestoda, Diphyllobothriidea), a human parasite with extreme fecundity. Parasitol Int. 2014;63:747–53. doi: 10.1016/j.parint.2014.07.002. PubMed DOI

Yoneva A, Scholz T, Bruňanská M, Kuchta R. Vitellogenesis of diphyllobothriidean cestodes (Platyhelminthes) C R Biol. 2015;338:169–79. doi: 10.1016/j.crvi.2015.01.001. PubMed DOI

Waeschenbach A, Webster BL, Littlewood DTJ. Adding resolution to ordinal level relationships tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogenet Evol. 2012;63:834–47. doi: 10.1016/j.ympev.2012.02.020. PubMed DOI

Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963;17:208–12. doi: 10.1083/jcb.17.1.208. PubMed DOI PMC

Kuchta R, Scholz T, Brabec J, Bray RA. Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. Int J Parasitol. 2008;38:49–55. doi: 10.1016/j.ijpara.2007.08.005. PubMed DOI

Smyth JD, McManus DP. The physiology and biochemistry of cestodes. Cambridge: Cambridge University Press; 1989.

Młocicki D, Świderski Z, Mackiewicz JS, Ibraheem MH. Ultrastructure of intrauterine eggs: evidence of early ovoviviparity in the caryophyllidean cestode Wenyonia virilis Woodland, 1923. Acta Parasitol. 2010;55:349–58.

Bruňanská M, Mackiewicz JS, Młocicki D, Świderski Z, Nebesářová J. Early intrauterine embryonic development in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae), an invasive tapeworm of carp (Cyprinus carpio): an ultrastructural study. Parasitol Res. 2012;110:1009–17. doi: 10.1007/s00436-011-2590-2. PubMed DOI

Młocicki D, Świderski Z, Eira C, Miquel J. An ultrastructural study of embryonic envelope formation in the anoplocephalid cestode Mosgovoyia ctenoides (Railliet, 1890) Beveridge, 1978. Parasitol Res. 2005;95:243–51. doi: 10.1007/s00436-004-1276-4. PubMed DOI

Świderski Z, Mackiewicz JS. Electron microscope study of vitellogenesis in Glaridacris catostomi (Cestoidea: Caryophyllidea) Int J Parasitol. 1976;6:61–73. doi: 10.1016/0020-7519(76)90011-4. PubMed DOI

Świderski Z, Bruňanská M, Poddubnaya LG, Mackiewicz JS. Cytochemical and ultrastructural study on vitellogenesis in caryophyllidean cestode Khawia armeniaca (Cholodkovski, 1915) Acta Parasitol. 2004;49:16–24.

Świderski Z, Młocicki D, Mackiewicz JS, Miquel J, Ibraheem MH, Bruňanská M. Ultrastructure and cytochemistry of vitellogenesis in Wenyonia virilis Woodland, 1923 (Cestoda, Caryophyllidea) Acta Parasitol. 2009;54:131–42.

Poddubnaya LG, Gibson DI, Świderski Z, Olson PD. Vitellocyte ultrastructure in the cestode Didymobothrium rudolphii (Monticelli, 1890): possible evidence for the recognition of divergent taxa within the Spathebothriidea. Acta Parasitol. 2006;51:255–63. doi: 10.2478/s11686-006-0039-z. DOI

Młocicki D, Świderski Z, Mackiewicz JS, Ibraheem M. Ultrastructural and cytochemical studies of GER-bodies in the intrauterine eggs of Wenyonia virilis Woodland, 1923 (Cestoda, Caryophyllidea) Acta Parasitol. 2011;56:40–7.

Bruňanská M, Drobníková P, Mackiewicz JS, Nebesářová J. Cytocomposition of the vitellarium in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae): another caryophyllidean species with lamellar bodies and lipids. Parasitol Res. 2013;112:2703–11. doi: 10.1007/s00436-013-3477-1. PubMed DOI

Bruňanská M, Drobníková P, Mackiewicz JS, Nebesářová J. Reinvestigation of vitellogenesis in Caryophyllaeus laticeps (Pallas, 1781) (Cestoda, Caryophyllidea, Caryophyllaeidae), monozoic tapeworm of Abramis brama (Pisces, Teleostei) Helminthologia. 2013;50:73–81.

Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, et al. Classification of cell death: recommendations of the nomenclature commitee on cell death 2009. Cell Death Differ. 2009;6:3–11. doi: 10.1038/cdd.2008.150. PubMed DOI PMC

Sperandio S, de Belle I, Bredesen DE. An alternative, nonapoptic form of programmed cell death. Proc Natl Acad Sci U S A. 2000;97:14376–81. doi: 10.1073/pnas.97.26.14376. PubMed DOI PMC

Wei T, Kang Q, Ma B, Gao S, Li X, Liu Y. Activation of autophagy and paraptosis in retinal ganglion cells after retinal ischemia and reperfusion injury in rats. Exp Ther Med. 2015;9:476–82. PubMed PMC

Smetana O, Široký J, Houlné G, Opatrný Z, Chabouté ME. Non-apoptotic programmed cell death with paraptotic-like features in bleomycin-treated plant cells is suppressed by inhibition of ATM/ATR pathways or NtE2F overexpression. J Exp Bot. 2012;63:2631–44. doi: 10.1093/jxb/err439. PubMed DOI

Hoa N, Myers MP, Douglass TG, Zhang JG, Delgado C, Driggers L, et al. Molecular mechanisms of paraptosis induction: implications for a non-genetically modified tumor vaccine. PLoS ONE. 2009;4(2):e4631. doi: 10.1371/journal.pone.0004631. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...