The immunobiological interplay between Pseudosuccinea columella resistant/susceptible snails with Fasciola hepatica: Hemocytes in the spotlight

Abstract

The Fasciola hepatica/Pseudosuccinea columella interaction in Cuba involves a unique pattern of phenotypes; while most snails are susceptible, some field populations are naturally resistant to infection and parasites are encapsulated by snail hemocytes. Thus, we investigated the hemocytes of resistant (R) and susceptible (S) P. columella, in particular morphology, abundance, proliferation and in vitro encapsulation activity following exposure to F. hepatica. Compared to susceptible P. columella, hemocytes from exposed resistant snails showed increased levels of spreading and aggregation (large adherent cells), proliferation of circulating blastlike cells and encapsulation activity of the hemocytes, along with a higher expression of the cytokine granulin. By contrast, there was evidence of a putative F. hepatica-driven inhibition of host immunity, only in susceptible snails. Additionally, (pre-)incubation of naïve hemocytes from P. columella (R and S) with different monosaccharides was associated with lower encapsulation activity of F. hepatica larvae. This suggests the involvement in this host-parasite interaction of lectins and lectins receptors (particularly related to mannose and fucose sensing) in association with hemocyte activation and/or binding to F. hepatica.

Immunological Resistance of Pseudosuccinea columella Snails From Cuba to Fasciola hepatica (Trematoda) Infection: What We Know and Where We Go on Comparative Molecular and Mechanistic Immunobiology, Ecology and Evolution

“…In this sense, histological sections of exposed resistant P. columella showed that the penetration of F. hepatica miracidium into the snail is rapidly followed by an effective encapsulation of the parasite larvae by the hemocytes of the host (circulating immune cells of snails), observed at 24 h post-exposure ( 28 ). This powerful immunological reaction is believed to be at the base of the resistance of P. columella to F. hepatica ( 17 , 28 ).…”

“…Although these attempts aimed at increasing the probability of encounter of compatible genotypic host–parasite individual combinations and at potentially decreasing the effectivity of the immune response of the host (such effects have been observed in susceptible populations used as control), they have all failed in rendering phenotypically resistant snails infected. Such stability and universality (at least at the above mentioned scale) of this phenotype paired to the potent immune response associated to it ( 17 , 28 ), point at the occurrence of an immunological resistance that is not restricted by specific interactions of matching genotypes between the host and the parasite. It is, therefore, rather a phenomenon of immunological resistance than one of incompatibility and that, noteworthy, has been selected in nature ( 18 , 28 ).…”

“…We have postulated that a major factor/function associated to a single locus or a few loci is present or highly abundant in the genetic clade of resistant P. columella snails. Such feature is believed to be involved proximately or ultimately, in the immunobiological interaction with F. hepatica , interfering with biologically relevant functions of the parasite coded by a single locus or a few loci highly conserved ( 17 ). Contrastingly, given the polymorphism of compatibility resulted from exposing different susceptible snails to different parasite isolates [see ( 12 , 13 ) for discussion], it was speculated that the major factor highly present in resistant snails is absent/scarce in susceptible P. columella and, consequently, it is the interplay among several other factors/functions between the susceptible host and the parasite that dictates the final outcome and the intensity of the infection, possibly preferentially following a matching allele model ( 17 ).…”

“…However, resistant populations have been only reported until now in specific natural field sites within the Caribbean island of Cuba and whenever tested, always succeed in fighting back the infection regardless of the F. hepatica isolate, the parasitic dose, or even the infection scheme used (e.g., ( 12 , 13 , 16 ). Immunological and molecular studies reflect a constitutively enhanced immune competence of resistant compared to susceptible populations ( 17 , 18 ), although such selection for resistance is thought to carry a cost in fitness in the absence of parasites; reproductive constraints have been associated to resistant P. columella ( 18 – 20 ). In this sense, distinctive ecological patterns have been related to each phenotype; in particular, resistant P. columella always occurs in relatively soft/acid waters with low malacological diversity ( 19 ).…”

Towards the comprehension of fasciolosis (re-)emergence: an integrative overview

“…On the intermediate host side, a few hours following infection, there is no significant haemocyte (snail immune cells) proliferation. In addition, lower expression of the proliferative cytokine granulin and lower levels of in vitro encapsulation activity (=protective immune response towards Fasciola ) of haemocytes against F. hepatica larvae have been found in susceptible over resistant Pseudosuccinea columella snails (Alba et al ., 2020).…”