Echinostoma paraensei: Hemocytes of Biomphalaria glabrata as targets of echinostome mediated interference with host snail resistance to Schistosoma mansoni

doi:10.1016/0014-4894(86)90018-4

Experimental Parasitology

Volume 62, Issue 1, August 1986, Pages 149-154

https://doi.org/10.1016/0014-4894(86)90018-4 Get rights and content

Abstract

Earlier in vivo work by Lie et al. (1977) indicated that the innate resistance of the 10R2 strain of Biomphalaria glabrata to PR1 Schistosoma mansoni could be interfered with if the snails were infected previously with another trematode, Echinostoma paraensei. We have studied this interference phenomenon using in vitro methods in an attempt to understand its mechanistic basis. Hemolymph, derived from 10R2 snails infected with E. paraensei for 14–28 days, killed 25% of S. mansoni sporocysts in vitro, significantly less (P < 0.001) than the 90% killing rate observed with hemolymph from uninfected, control 10R2 snails. Hemolymph from the infected 10R2 snails and from schistosome susceptible M line snails did not differ significantly (P > 0.1) in their relative inability to kill S. mansoni sporocysts in vitro. The defect in sporocyst killing exhibited by echinostome infected 10R2 snails was traced to the cellular, rather than the humoral, component of the hemolymph. Preparations containing uninfected 10R2 snail hemolymph and echinostome daughter rediae exhibited significantly less (P < 0.001) killing of S. mansoni sporocysts than did controls containing only 10R2 hemolymph and S. mansoni sporocysts. Our results suggest that echinostome larvae release factors that interfere with the ability of B. glabrata hemocytes to kill S. mansoni sporocysts.

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Host exposure history and priority effects impact the development and reproduction of a dominant parasite
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Within a single organism, numerous parasites often compete for space and resources. This competition, together with a parasite’s ability to locate and successfully establish in a host, can contribute to the distribution and prevalence of parasites. Coinfection with trematodes in snail intermediate hosts is rarely observed in nature, partly due to varying competitive abilities among parasite taxa. Using a freshwater snail host (Biomphalaria glabrata), we studied the ability of a competitively dominant trematode, Echinostoma caproni, to establish and reproduce in a host previously infected with a less competitive trematode species, Schistosoma mansoni. Snails were exposed to S. mansoni and co-exposed to E. caproni either simultaneously or 1 week, 4 weeks, or 6 weeks post S. mansoni exposure. Over the course of infection, we monitored the competitive success of the dominant trematode through infection prevalence, parasite development time, and parasite reproductive output. Infection prevalence of E. caproni did not differ among co-exposed groups or between co-exposed and single exposed groups. However, E. caproni infections in co-exposed hosts took longer to reach maturity when the timing between co-exposures increased. All co-exposed groups had higher E. caproni reproductive output than single exposures. We show that although timing of co-exposure affects the development time of parasite transmission stages, it is not important for successful establishment. Additionally, co-exposure, but not priority effects, increases the reproductive output of the dominant parasite.
Changes in hemocytes of Biomphalaria glabrata infected with Echinostoma paraensei and exposed to glyphosate-based herbicide
2019, Journal of Invertebrate Pathology
Citation Excerpt :
The freshwater snail Biomphalaria glabrata Say, 1818 (Gastropoda: Planorbidae) is an important intermediate host for the larval developmental stages of different parasitic platyhelminths (flatworms), including Schistosoma mansoni Sambon, 1907 and Echinostoma paraensei Lie and Basch, 1967 (Lie and Basch, 1967; Loker et al., 1986; Paraense, 2001).
The immune system of snails is highly sensitive to pollutants, which can suppress its immune response. We investigated the effects of exposure to the glyphosate-based herbicide Roundup® Original on the snail Biomphalaria glabrata infected by the platyhelminth Echinostoma paraensei by evaluating changes in the snail’s internal defense system. Four cohorts were studied: control group, infected snails, snails treated with Roundup®, and snails infected and treated with Roundup®. The hemocyte viability was assessed, morphological differentiation of cells was observed and flow cytometry was performed to determine the morphology, viability and the lectin expression profiles. The frequencies of dead hemocytes were lower in the infected group and higher in both pesticide treated groups. Three cell types were identified: blast-like cells, hyalinocytes and granulocytes. The highest number of all types of hemocytes, as well as the highest number of dead cells, were observed in the infected, pesticide-treated group. The association between infection and herbicide exposure greatly increased the frequency of dead hemocytes, suggesting that this condition impairs the internal defense system of B. glabrata making the snails more vulnerable to parasitic infections.
Proteomic profile of Bithynia siamensis goniomphalos snails upon infection with the carcinogenic liver fluke Opisthorchis viverrini
2015, Journal of Proteomics
The snail Bithynia siamensis goniomphalos acts as the first intermediate host for the human liver fluke Opisthorchis viverrini, the major cause of cholangiocarcinoma (CCA) in Northeast Thailand. The undisputed link between CCA and O. viverrini infection has precipitated efforts to understand the molecular basis of host–parasite interactions with a view to ultimately developing new control strategies to combat this carcinogenic infection. To date most effort has focused on the interactions between the parasite and its human host, and little is known about the molecular relationships between the liver fluke and its snail intermediate host. In the present study we analyse the protein expression changes in different tissues of B. siamensis goniomphalos induced by infection with larval O. viverrini using iTRAQ labelling technology. We show that O. viverrini infection downregulates the expression of oxidoreductases and catalytic enzymes, while stress-related and motor proteins are upregulated. The present work could serve as a basis for future studies on the proteins implicated in the susceptibility/resistance of B. siamensis goniomphalos to O. viverrini, as well as studies on other pulmonate snail intermediate hosts of various parasitic flukes that infect humans.
Despite the importance and high prevalence of opisthorchiasis in some regions of Southeast Asia and the direct relationship between infection by Opisthorchis viverrini and the incidence of cholangiocarcinoma, little is known of the modifications induced by this parasite in its snail intermediate hosts. This time-course study provides the first in-depth quantitative proteomic analysis of experimentally infected Bithynia siamensis goniomphalos. We show how motor and stress-related proteins are upregulated in infected snails, while O. viverrini infection downregulates the expression of oxidoreductases and catalytic enzymes. This work serves as a basis for the development of new strategies, focused on the invertebrate intermediate hosts, to control parasite transmission.
Effect of a hemiuroid trematode on the hemocyte immune parameters of the cockle Anadara trapezia
2013, Fish and Shellfish Immunology
Citation Excerpt :
For example, changes may occur in the number, morphology, and phagocytic activity of the hemocytes, such as in the snail B. glabrata following infection with S. mansoni[15], and in Lymnaea stagnalis when infected with Trichobilharzia ocellata [16]. These modifications of the immune system following infection of a susceptible host seem to be species-specific [17]. The current study considered the marine bivalve Anadara trapezia and its cellular immune responses to asexual stages of a hemiuroid trematode by comparing hemocyte parameters in parasitized and non-parasitized cockles using histology and flow cytometry.
When a trematode parasite penetrates a potential molluscan host, it has to circumvent the host's internal defense system. In molluscs, the primary effector cells of this system are the hemocytes which orchestrate many of the cellular and humoral immune functions. Survival of the parasite can occur only in the absence of a successful immune response, and continued development only if the host is physiologically suitable. This study investigated hemocytic response against asexual stages of a hemiuroid trematode by its host, the marine bivalve Anadara trapezia. Hemocyte characteristic (type, morphology) and function (mortality, phagocytosis and oxidative activity) were analyzed by flow cytometry in parasitized and non-parasitized cockles. A. trapezia possesses two types of hemocytes: amebocytes and erythrocytes. Analysis of histological section showed that there was no host hemocytic response around hemiuroid sporocysts. The infection induced a significant increase of the total circulating hemocytes with a higher proportion of erythrocytes relative to amebocytes, coupled with a lower phagocytosis rate and a statistically non-significant decrease of the intracellular oxidative activity. No significant differences were observed in hemocyte size and complexity, mortality, or phagocytic capacity. Our results indicate that in A. trapezia, hemiuroids modulate the immune response by increasing the number of circulating hemocytes and decreasing phagocytosis.
Tissue responses exhibited by Biomphalaria alexandrina snails from different Egyptian localities following Schistosoma mansoni exposure
2011, Experimental Parasitology
Citation Excerpt :
Many investigators observed cellular reaction against trematode invasion such reactions usually consist of massive proliferation of amebocytes, with encapsulation and destruction of sporocysts (Pan, 1965; Bayne et al., 1980). Similarly Loker et al. (1986) found miracidium–amebocyte contact within 3 h and phagocytosis of sporocysts microvilli and pieces of tegument within 7.5 h, while extensive pathology was demonstrated within 24 h and by 48 h only scattered remnants of sporocysts remained. Hemocytes contact with sporocysts is essentials for rapid sporocysts death in vivo and most sporocysts of S. mansoni were dead within 72 h (Sullivan and Hu, 1995).
Snails’ susceptibilities to infection with Schistosoma mansoni were determined through observation of infection rates, total cercarial production and tissue responses of the first generation (F1) of Biomphalaria alexandrina snails, originally collected from different Egyptian governorates (Giza, Fayoum, Kafr El-Sheikh, Ismailia and Damietta) and responses were compared between groups. The emergence of cercariae for a 3-month period and the calculation of survival and infection rates, in control (Schistosome Biological Supply Center; SBSC) and infected snails were evaluated. SBSC and Giza snails showed greater susceptibilities to infection and lower mortality rates. In addition, at 6 and 72 h post-exposure to miracidia all the snail groups showed no difference in the anatomical locations of sporocysts. The larvae were found in the head-foot, the mantle collar and the tentacles of the snails. Sporocysts showed normal development with low tissue reactions in SBSC and Giza snail groups infected with S. mansoni miracidia (SBSC). However, in Fayoum, Kafr El-Sheikh, Ismailia and Damietta snail groups, variable tissue responses were observed in which numerous hemocytes made direct contact with S. mansoni larvae forming capsules. The results suggested that, different responses of B. alexandrina snail’s hemocytes towards S. mansoni are related to the degree of susceptibility of these snails. So this is important in planning the strategy of schistosomiasis control.
Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei
2010, International Journal for Parasitology
Successful colonization of a compatible snail host by a digenetic trematode miracidium initiates a complex, proliferative development program requiring weeks to reach culmination in the form of production of cercariae which, once started, may persist for the remainder of the life span of the infected snail. How are such proliferative and invasive parasites able to circumvent host defenses and establish chronic infections? Using a microarray designed to monitor the internal defense and stress-related responses of the freshwater snail Biomphalaria glabrata, we have undertaken a time course study to monitor snail responses following exposure to two different trematode species to which the snail is susceptible: the medically important Schistosoma mansoni, exemplifying sporocyst production in its larval development, or Echinostoma paraensei, representing an emphasis on rediae production in its larval development. We sampled eight time points (0.5, 1, 2, 4, 8, 16 and 32 days p.i.) that cover the period required for cercariae to be produced. Following exposure to S. mansoni, there was a preponderance of up-regulated over down-regulated array features through 2 days p.i. but by 4 days p.i. and thereafter, this pattern was strongly reversed. For E. paraensei, there was a preponderance of down-regulated array features over up-regulated features at even 0.5 days p.i., a pattern that persists throughout the course of infection except for 1 day p.i., when up-regulated array features slightly outnumbered down-regulated features. Examination of particular array features revealed several that were up-regulated by both parasites early in the course of infection and one, fibrinogen related protein 4 (FREP 4), that remained significantly elevated throughout the course of infection with either parasite, effectively serving as a marker of infection. Many defense-related transcripts were persistently down-regulated, including several fibrinogen-containing lectins and homologs of molecules best known from vertebrate phagocytic cells. Our results are consistent with earlier studies suggesting that both parasites are able to interfere with host defense responses, including a tendency for E. paraensei to do so more rapidly and strongly than S. mansoni. They further suggest mechanisms for how trematodes are able to establish the chronic infections necessary for their continued success.

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¹: Present address: Biology Department, University of New Mexico, Albuquerque, New Mexico 87131, USA.

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Experimental Parasitology

Abstract

References (18)

Schistosoma mansoni: Immunofluorescent detection of its antigen reacting with Biomphalaria glabrata amoebocytes

Experimental Parasitology

Schistosoma mansoni: Cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata

Experimental Parasitology

Schistosoma mansoni: Lectin-dependent cytotoxicity of hemocytes from susceptible host snails, Biomphalaria glabrata

Experimental Parasitology

Studies on resistance in snails: Interference by nonirradiated echinostome larvae with natural resistance to Schistosoma mansoni in Biomphalaria glabrata

Journal of Invertebrate Pathology

Intramolluscan inter-trematode antagonism: Review of factors influencing the host-parasite system and its possible role in biological control

Advances in Parasitology

Schistosoma mansoni: Agglutination of sporocysts, and formation of gels on miracidia transforming in plasma of Biomphalaria glabrata

Experimental Parasitology

Schistosome sporocyst-killing cells isolated from Biomphalaria glabrata

Journal of Invertebrate Pathology

Predation by echinostome rediae upon schistosome sporocysts in vitro

Journal of Parasitology

Macrophagelike hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro

Journal of Parasitology

Cited by (48)

Host exposure history and priority effects impact the development and reproduction of a dominant parasite

Changes in hemocytes of Biomphalaria glabrata infected with Echinostoma paraensei and exposed to glyphosate-based herbicide

Proteomic profile of Bithynia siamensis goniomphalos snails upon infection with the carcinogenic liver fluke Opisthorchis viverrini

Effect of a hemiuroid trematode on the hemocyte immune parameters of the cockle Anadara trapezia

Tissue responses exhibited by Biomphalaria alexandrina snails from different Egyptian localities following Schistosoma mansoni exposure

Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei