Abstract
BackgroundPhagocyte-derived extracellular traps (ETs) were recently demonstrated mainly in vertebrate hosts as an important effector mechanism against invading parasites. In the present study we aimed to characterize gastropod-derived invertebrate extracellular phagocyte trap (InEPT) formation in response to larval stages of important canine and feline metastrongyloid lungworms. Gastropod haemocytes were isolated from the slug species Arion lusitanicus and Limax maximus, and the snail Achatina fulica, and exposed to larval stages of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Troglostrongylus brevior and investigated for gastropod-derived InEPT formation.ResultsPhase contrast as well as scanning electron microscopy (SEM) analyses of lungworm larvae-exposed haemocytes revealed ET-like structures to be extruded by haemocytes thereby contacting and ensnaring the parasites. Co-localization studies of haemocyte-derived extracellular DNA with histones and myeloperoxidase in larvae-entrapping structures confirmed classical characteristics of ETs. In vivo exposure of slugs to A. vasorum larvae resulted in InEPTs being extruded from haemocytes in the slug mucous extrapallial space emphasizing the pivotal role of this effector mechanism against invasive larvae. Functional larval entrapment assays demonstrated that almost half of the haemocyte-exposed larvae were contacted or even immobilized by released InEPTs. Overall, as reported for mammalian-derived ETs, different types of InEPTs were here observed, i.e. aggregated, spread and diffused InEPTs.ConclusionsTo our knowledge, this study represents the first report on metastrongyloid lungworm-triggered ETosis in gastropods thereby providing evidence of early mollusc host innate immune reactions against invading larvae. These findings will contribute to the better understanding on complex parasite-intermediate host interactions since different gastropod species bear different transmitting capacities for metastrongyloid infections.
Highlights
Phagocyte-derived extracellular traps (ETs) were recently demonstrated mainly in vertebrate hosts as an important effector mechanism against invading parasites
Metastrongyloid lungworm larvae induce gastropod invertebrate extracellular phagocyte trap (InEPT) in a parasite species- and stage-independent manner Microscopic analyses revealed that exposure of first- and third-stage larvae of A. vasorum to gastropod haemocytes trigger the formation of ET-like structures indicating a stage-independent process (Additional file 1) since both larval stages (L1, Third-stage larvae (L3)) were attacked by InEPTs
To account for parasite-specificity we tested A. abstrusus- and T. brevior-First-stage larvae (L1) for their capability to induce InEPTs and both parasite species triggered InEPT formation in exposed haemocytes. These data clearly provide evidence against a parasite-specificity of metastrongyloid-triggered InEPT formation highlighting the capacity of gastropod haemocytes to react to different lungworm parasites the reaction is species-independent
Summary
Phagocyte-derived extracellular traps (ETs) were recently demonstrated mainly in vertebrate hosts as an important effector mechanism against invading parasites. In the last decade canine and feline lungworm species such as Angiostrongylus vasorum, Aelurostrongylus abstrusus and Troglostrongylus brevior are emerging in several countries and spreading into previously nonreported areas [5,6,7,8,9,10,11,12] The former parasite induces a debilitating disease of the cardiorespiratory system [5, 13] but can cause neurological, ophthalmic and systemic disease with sometimes life threatening coagulopathies in dogs. Haemocytes were reported to be involved in several physiological functions such as wound repair, coagulation, transport of nutrients and other molecules and intracellular digestion [15, 16] Overall, this cell type is known as the key player of the molluscan innate immune system [17]. The detailed molecular mechanisms of these immunological processes are not well understood, so far [18,19,20,21,22]
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