Secretory glands in cercaria of the neuropathogenic schistosome Trichobilharzia regenti - ultrastructural characterization, 3-D modelling, volume and pH estimations

Abstract

BackgroundCercariae of schistosomes employ bioactive molecules for penetration into their hosts. These are released from specialized unicellular glands upon stimuli from host skin. The glands were previously well-described in the human pathogen Schistosoma mansoni. As bird schistosomes can also penetrate human skin and cause cercarial dermatitis, our aim was to characterize the architecture and ultrastructure of glands in the neurotropic bird schistosome Trichobilharzia regenti and compare it with S. mansoni. In the context of different histolytic enzymes used by these two species, we focused also on the estimations of gland volumes and pH in T. regenti.ResultsThe architecture and 3-D models of two types of acetabular penetration glands, their ducts and of the head gland are shown here. We characterized secretory vesicles in all three gland types by means of TEM and confirmed accuracy of the models obtained by confocal microscopy. The results of two independent approaches showed that the glands occupy ca. one third of cercarial body volume (postacetabular glands ca. 15%, circumacetabular 12% and head gland 6%). The inner environment within the two types of acetabular glands differed significantly as evidenced by dissimilar ability to bind fluorescent markers and by pH value which was higher in circumacetabular (7.44) than in postacetabular (7.08) glands.ConclusionsAs far as we know, this is the first presentation of a 3-D model of cercarial glands and the first exact estimation of the volumes of the three gland types in schistosomes. Our comparisons between T. regenti and S. mansoni implied that the architecture and ultrastructure of the glands is most likely conserved within the family. Only minor variations were found between the two species. It seems that the differences in molecular composition have no effect on general appearance of the secretory cells in TEM. Fluorescent markers employed in this study, distinguishing between secretory vesicles and gland types, can be useful in further studies of mechanisms used by cercariae for host invasion. Results of the first attempts to estimate pH within schistosome glands may help further understanding of regulation of enzymatic activities present within the glands.

Trichobilharzia regenti: Antigenic structures of intravertebrate stages

“…Cercarial secretory products released from the penetration glands are essential for glycocalyx shedding and parasite penetration through the host tissues [18,19], and molecules contained in these products represent immunogens able to induce a strong antibody response and bias the immune response to Th2 polarization [5]. Cercarial glands occupy approximately one third of cercarial body volume and their products consist of a large amount of material [20], nevertheless, the molecules acting as immunogens may represent a small portion of cercarial gland content. This could explain only sporadic binding of antibody.…”

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…12%). Differences were observed in the appearance of granular material/secretory vesicles contained in the glands, pH value, and the ability to bind various dyes and fluorescent markers (180,182).…”

A next-generation microarray further reveals stage-enriched gene expression pattern in the blood fluke Schistosoma japonicum

“…Collectively, the upregulated expression of these genes in cercariae indicates that signal transduction (ribosomal protein S6 kinase beta-2 [42]), vesicular trafficking (calcium-dependent secretion activator [43] and small GTPase Rab-protein 11 [44]) and energy metabolism (AMP deaminase [45] and 5′-AMP-activated protein kinase [46]) and transcriptional regulation (krueppel-like factor 11, homeobox protein SMOX-1, and retinoid X receptor RXR-2) are active processes in this stage.…”