Influence of Trichobilharzia regenti (Digenea: Schistosomatidae) on the defence activity of Radix lagotis (Lymnaeidae) Haemocytes.

Vladimír Skála,Anthony J Walker,Zuzana Jindrová,Martin Kašný,Alena Černíková,Petr Horák,Martin Vostrý,Daniel Doucet

doi:10.1371/journal.pone.0111696

Abstract

Radix lagotis is an intermediate snail host of the nasal bird schistosome Trichobilharzia regenti. Changes in defence responses in infected snails that might be related to host-parasite compatibility are not known. This study therefore aimed to characterize R. lagotis haemocyte defence mechanisms and determine the extent to which they are modulated by T. regenti. Histological observations of R. lagotis infected with T. regenti revealed that early phases of infection were accompanied by haemocyte accumulation around the developing larvae 2–36 h post exposure (p.e.) to the parasite. At later time points, 44–92 h p.e., no haemocytes were observed around T. regenti. Additionally, microtubular aggregates likely corresponding to phagocytosed ciliary plates of T. regenti miracidia were observed within haemocytes by use of transmission electron microscopy. When the infection was in the patent phase, haemocyte phagocytic activity and hydrogen peroxide production were significantly reduced in infected R. lagotis when compared to uninfected counterparts, whereas haemocyte abundance increased in infected snails. At a molecular level, protein kinase C (PKC) and extracellular-signal regulated kinase (ERK) were found to play an important role in regulating these defence reactions in R. lagotis. Moreover, haemocytes from snails with patent infection displayed lower PKC and ERK activity in cell adhesion assays when compared to those from uninfected snails, which may therefore be related to the reduced defence activities of these cells. These data provide the first integrated insight into the immunobiology of R. lagotis and demonstrate modulation of haemocyte-mediated responses in patent T. regenti infected snails. Given that immunomodulation occurs during patency, interference of snail-host defence by T. regenti might be important for the sustained production and/or release of infective cercariae.

Highlights

Aquatic snails serve as intermediate hosts of many trematodes, including those important in veterinary and human medicine
Histological observations of R. lagotis experimentally infected with T. regenti provided insights into the encapsulation responses within the snail tissue between 1 and 92 h p.e
Histological observation of T. regenti in R. lagotis We evaluated by histology haemocyte migratory/encapsulation responses triggered in R. lagotis by the bird schistosome, T. regenti

Summary

Introduction

Aquatic snails serve as intermediate hosts of many trematodes, including those important in veterinary and human medicine. Compatibility between such parasites and the host snail is partially governed by innate immunological processes that comprise cellular and humoral components. Haemocytemediated defence responses that are important for eliminating foreign invaders such as parasites include phagocytosis, encapsulation, and production of reactive oxygen species (ROS) [1], [3], [4]. Activation of PKC, p38 MAPK and/or extracellular signal-regulated kinase (ERK) is required for efficient phagocytosis and H2O2 production by snail haemocytes; other kinases such as phosphatidylinositol 3kinase play a crucial role in these processes [7], [9,10,11,12]

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