Experimental study of ultrastructural mechanisms and kinetics of tegumental secretion in cestodes parasitizing fish (Cestoda: Diphyllobothriidea)

Abstract

The structural response and plasticity of the cestode tegument in response to the influence of the host organism is not yet well understood. The main aims of our in vitro study were to analyse the ultrastructural mechanisms and kinetics of tegumental secretion in two cestode species, Dibothriocephalus dendriticus and Ligula interrupta, in response to the influence of fish host blood serum. The incubation of plerocercoids in the culture medium, which contained fish host blood serum, resulted in an increased number of secretory products on the tegumental surface. Our study is the first to experimentally demonstrate the formation of plerocercoid protective layers influenced by the host's internal environment factors. The mechanism of the generation of the protective layer included the following: the intensive formation of organelles in the tegumental cytons and their transfer to the distal cytoplasm of the tegument; increases in extracellular vesicles and vacuoles released on the tegumental surface; arrangement of secretory products and fine‐dispersed extracellular matrix in layers; and formation of the protective layer. The structural tegumental response included increases in the glycocalyx layer and structural changes. Our study revealed that the universal mechanism of protective layer formation was intrinsic to different tapeworms. We hypothesize that plerocercoids of cestodes parasitizing fish may use tegumental secretion in the formation of a protective layer and in the release of immunoregulator molecules to evade the host's immune response.

Tegument Ultrastructure and Morphology of the Capsule Surrounding the Tetrathyridia of the Genus Mesocestoides Vaillant, 1863 in the Liver of the Root Vole

“…The appearance of shed microtriches, which, as in our case, looked like vacuoles with dense walls [ 42 ] but were located in a layered manner over the microtrichial border, was also attributed to the effect of serum. The layered arrangement of the material secreted by the tegument of cestodes was noted in several species [ 42 , 45 , 50 ]. Most clearly it is represented in cystic echinococci in the form of a laminated layer surrounding the cyst [ 51 ].…”

“…Despite the methodological complexity of study, the excretory–secretory processes in helminths draw particular attention, given the possibility of using the results of such studies for practical purposes [ 46 , 50 , 53 – 56 ]. The authors of some of the above-cited works pay special attention to the extracellular vesicles released from the surface of parasites, and it cannot be ruled out that that the chains of vesicles noted by us carry substances with immunomodulatory properties.…”

Investigation of excretory/secretory products from gull-tapeworm Dibothriocephalus dendriticus and ligula Ligula interrupta plerocercoids anti-inflammatory properties

“…Получены первые данные по распределению простагландина Е 2 , серотонина, гамма-аминомасляной кислоты, пептида Phe-Met-Arg-Phe-NH 2 в организме Dibothriocephalus dendriticus (Nitzsch, 1824) [13][14][15][16]. Изучены ультраструктурные механизмы и кинетика вывода секрета на поверхность тегумента цестод D. dendriticus и Ligula interrupta (Rudolphi, 1810) в ответ на стимуляцию сывороткой крови хозяев -рыб [17].…”

New Gland Type Discovered in Cestodes: Neurosecretory Neurons Release a Secret into the Fish Host

“…Nutrients are absorbed through a syncytial outer tissue known as the tegument. A complex mixture of excretory and secretory products, which are collectively termed the secretome, is known to be released by a parasite [1][2][3]. Terminals of frontal glands penetrate the tegument together with free nerve endings, which are separated from the tegument membrane by a system of specialized contacts.…”

“…Ultrastructural studies were performed by transmission electron microscopy, using techniques modified to study cestodes [ 8 , 12 , 13 ]. To assess the changes in activity of secretion from the free terminal surface in D. dendriticus and L. interrupta , experiments were carried out according to a protocol developed previously [ 3 ].…”