Influence of Trichobilharzia regenti (Digenea: Schistosomatidae) on the Defence Activity of Radix lagotis (Lymnaeidae) Haemocytes

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.

Snail defence responses to parasite infection: The Lymnaea stagnalis-Trichobilharzia szidati model

“…), haemocyte peroxidase and phagocytic activities increased again (Amen et al, 1991a;Amen et al, 1992a), whereas Horák and Deme (1998) reported just minor differences between the infected snails and uninfected control L. stagnalis snails in terms of haemocyte phagocytic activity at ten weeks p.i. Contrary to these observations, phagocytic activity and capacity to generate hydrogen peroxide were suppressed in haemocytes from R. lagotis in the patent phase of infection with T. regenti (Skála et al, 2014). Moreover, these haemocytes displayed lower PKC and ERK activity when compared to those from uninfected snails.…”

“…Moreover, these haemocytes displayed lower PKC and ERK activity when compared to those from uninfected snails. Considering the regulatory role of these pathways in haemocyte defence processes, this suggests how the parasite may achieve suppression of haemocyte defence activities in infected snails (Skála et al, 2014). In addition, the size distribution of circulating haemocytes in L. stagnalis was unaffected by T. szidati as revealed by flow cytometry at two, four, six, and eight weeks p.i.…”

“…with T. szidati, the IDS of L. stagnalis is clearly activated as shown by enhanced phagocytosis of zymosan particles or Aeromonas salmonicida bacteria by haemocytes in vitro (Amen and de Jong-Brink 1992;Amen et al, 1992a;Nuñez et al, 1994). Such activation is likely triggered by the shed miracidial ciliated plates (Amen et al, 1992a) that are highly antigenic and have been observed within phagosomes of haemocytes of another lymnaeid snail species (Radix lagotis) after infection Journal Pre-proof with another species of avian schistosome, Trichobilharzia regenti (Skála et al, 2014).…”

Extracellular trap-like fiber release may not be a prominent defence response in snails: evidence from three species of freshwater gastropod molluscs

“…1H). This finding was unexpected because PMA induces the respiratory burst in R. lagotis haemocytes (Skála et al, 2014), a reaction considered essential for ET-like fiber formation (Robb et al, 2014;Poirier et al, 2014).…”

“…Experiments with P. corneus were also conducted in Chernin´s balanced salt solution (CBSS; Chernin, 1963). Haemolymph from R. lagotis was handled as described previously (Skála et al, 2014). The haemocyte number per well was approx.…”