Elsevier

Acta Tropica

Volume 64, Issues 1–2, 1 April 1997, Pages 5-17
Acta Tropica

Review
The early stages of Echinococcus granulosus development

https://doi.org/10.1016/S0001-706X(96)00636-5Get rights and content

Abstract

The paper points out the essential aspects of host/parasite relationship during the development of oncospheres (ONC) of Echinococcus granulosus into an early cyst. Secretions of the penetration glands in the hatched ONC causes lysis of host tissue during penetration of the activated ONC. It also protects the parasite against the host's immune response while developing the laminated layer. The microvilli, compressed under the plasma membrane in the hatched ONC, are uplifted in the activated larvae; they increase in number and size and are substituted by short and truncated microtriches in metacestodes 3 days old. At that time appears the first lamination of the laminated layer that surrounds the metacestodes as an electron-dense matrix composed of fine microfibrillated material and remnants of sloughed microvilli. The second lamination appears by day 6–8 and is more electron-dense than the first one. The laminated layer is of parasite origin, formed of a series that emanates from the germinal membrane. It is suggested that Vg secretory vesicles, that are elaborated in the perikaryon of the germinal zone and continuously carried to the syncytium via the microtubular cytoskeleton, are responsible for the laminated layer formation and are involved in initial evasion of the immune response of the host. The cyclical production of laminations could be necessary to create layers that can ultimately be sloughed off as the cyst grows and serve to divert the host cellular response to the parasite.

Introduction

Human cystic echinococcosis (CE) is a cyclozoonotic infection produced by the larval stage (metacestode) of Echinococcus granulosus. It has a world-wide distribution with endemic foci in each inhabited continent (Matossian et al., 1977; Rausch, 1986; Eckert and Thompson, 1988; Schantz et al., 1995) and constitutes a major economic and health problem (McManus and Smyth, 1986; Schwabe, 1986).

The knowledge of post-oncospheral differentiation is essential for the comprehension of the host-parasite relationship since structural changes of the developing hydatid cyst tegument may reflect the parasite's immunoprotective mechanism (Holcman et al., 1994). In CE, the oncosphere of E. granulosus plays a central role in research on echinococcosis control. The oncosphere is the first invasive form recognized by the intermediate host's immune reactions and becomes also a target of the early responses. Since oncosphere that develop into cyst must evade the host immune system, ultrastructural studies of the tegumentary differentiation may elucidate the survival mechanism of the parasite.

The tegument is a complex living structure involved in penetration of the host intestine, absorption of nutrients, and stimulation of the host immune response (protective antibodies are active on the microvilli of the metacestodes). The essential host-parasite interface is at the parasite plasma membrane, and it is the immune recognition at this site that must initiate the parasite rejection by whatever mechanism (Ortega-Pierres et al., 1984). The plasma membrane of oncospheral epithelium is the obvious site of both functional antigen expression and of complement-mediated lysis in the host (Heath et al., 1994). It has been shown that successful immunoprophylaxis is feasible on the basis of oncosphere-derived antigens (Heath, 1986, Heath, 1995).

Section snippets

Development from the egg to an oncosphere

The following review is based on the ultrastructure of epithelial changes during the first 5 (Holcman et al., 1994) and 8 (Harris et al., 1989) days of the E. granulosus development. Figures are taken from Holcman et al. (1994).

Mature E. granulosus eggs have a thick embryophore and its ultrastructure shows it is made of thick elongated blocks united by electron-lucid cement (Fig. 1) and the oncosphere membrane is a thin cytoplasmic layer surrounding the oncosphere. In the hatched oncosphere (

Post-oncospheral development

The post-oncospheral development is a complex process of cytodifferentiation difficult to be observed in vivo.

There is a great number of studies on in vitro culture of protoscoleces from fertile hydatid cysts to adult strobilate stage and a significant number on the ultrastructure of E. granulosus protoscolex tegument and of the germinal and laminated layers of the hydatid cyst (Morseth, 1967; Bortoletti and Ferretti, 1973, Bortoletti and Ferretti, 1978; Lascano et al., 1975; Conder et al., 1983

The mature cyst

The developed metacestode is an unilocular cyst and could attain large size. The cavity of the cyst is filled with sterile hydatid fluid, which is a complex mixture of parasite-derived molecules and host-derived serum components (reviewed by Rickard and Lightowlers, 1986; McManus and Bryant, 1995). The cyst wall consists of an inner thin multinucleated germinal layer and an outer thick acellular laminated layer. The laminated layer is made up of a number of laminations and besides giving

Conclusions

This review intended to point out that early stages of metacestode development are still scarcely elucidated in the literature. Further studies on morphogenesis of the surface epithelium could lead to a better understanding of the essential aspects of host/parasite relationship in cystic echinococcosis. It was shown that the laminated layer, which is presumed to protect the parasite from the host's immune response, is of parasite origin. Assuming that the Vg secretory vesicles are responsible

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