In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens

Franke, Frederik; Rahn, Anna K.; Dittmar, Janine; Erin, Noémie I.; Rieger, Jennifer K.; Haase, David; Samonte-Padilla, Irene E; Lange, Joseph; Jakobsen, Per Johan; Hermida, Miguel; Fernández, Carlos; Kurtz, Joachim; Bakker, Theo C. M.; Reusch, Thorsten B. H.; Kalbe, Martin; Scharsack, Jörn P.

doi:10.1016/j.fsi.2013.10.019

Cited by 29 publications

(34 citation statements)

References 59 publications

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“…Parasitic helminths in natural habitats can drastically reduce their host fitness, and accordingly the hosts have evolved powerful counter-measures to control infection [38]. It is reasonable to concur with the statement of Secombes & Chappell [39] and Franke et al [40] that the successful infection of helminths largely depends on their capacity to evade and/or manipulate the generally efficient immune system of hosts. In recent years there has been a renaissance in the study of fish immune responses [27, 41–43], which significantly expanded our knowledge of the evolution and diversification of the vertebrate immune system [44, 45].…”

Section: Discussionmentioning

confidence: 90%

Nematode infection in liver of the fish Gymnotus inaequilabiatus (Gymnotiformes: Gymnotidae) from the Pantanal Region in Brazil: pathobiology and inflammatory response

et al. 2016

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BackgroundA survey on endoparasitic helminths from freshwater fishes in the Pantanal Region (Mato Grosso do Sul, Brazil) revealed the occurrence of third-larval stage of the nematode Brevimulticaecum sp. (Heterocheilidae) in most organs of Gymnotus inaequilabiatus (Gymnotidae) also known by the local name tuvira. The aim of the present study was to examine Brevimulticaecum sp.-infected tuvira liver at the ultrastructural level and clarify the nature of granulomas and the cellular elements involved in the immune response to nematode larvae.MethodsThirty-eight adult specimens of tuvira from Porto Morrinho, were acquired in January and March 2016. Infected and uninfected liver tissues were fixed and prepared for histological and ultrastructure investigations.ResultsThe prevalence of infection of tuvira liver by the nematode larvae was 95 %, with an intensity of infection ranging from 4 to 343 larvae (mean ± SD: 55.31 ± 73.94 larvae per liver). In livers with high numbers of nematode larvae, almost entire hepatic tissue was occupied by the parasites. Hepatocytes showed slight to mild degenerative changes and accumulation of pigments. Parasite larvae were surrounded by round to oval granulomas, the result of focal host tissue response to the infection. Each granuloma was typically formed by three concentric layers: an outer layer of fibrous connective tissue with thin elongated fibroblasts; a middle layer of mast cells entrapped in a thin fibroblast-connective mesh; and an inner layer of densely packed epithelioid cells, displaying numerous desmosomes between each other. Numerous macrophage aggregates occurred in the granulomas and in the parenchyma.ConclusionsOur results in tuvira showed that the larvae were efficiently sequestered within the granulomas, most of the inflammatory components were confined within the thickness of the granuloma, and the parenchyma was relatively free of immune cells and without fibrosis. Presumably this focal encapsulation of the parasites permits uninfected portions of liver to maintain its functions and allows the survival of the host.

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Section: Discussionmentioning

confidence: 90%

Nematode infection in liver of the fish Gymnotus inaequilabiatus (Gymnotiformes: Gymnotidae) from the Pantanal Region in Brazil: pathobiology and inflammatory response

et al. 2016

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“…Although we found that LPS-treated fish spent significantly less time near a shoal than CTRL fish, we did not find any significant changes in the other behaviours. One possible explanation could be that fish immune systems are unable to recognize LPS (Seppola et al, 2015); however, both LPS and S. solidus antigens increase head kidney leucocyte activity of sticklebacks (Franke et al, 2014), suggesting that LPS does induce a response in this species. This result must nonetheless be viewed in the context of pathogen specificity of the immune response.…”

Section: The Host Immune Response Hypothesismentioning

confidence: 99%

Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?

Hébert

Berger

Barber

et al. 2016

Journal of Experimental Biology

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Sticklebacks infected by the parasitic flatworm Schistocephalus solidus show dramatic changes in phenotype, including a loss of species-typical behavioural responses to predators. The timing of host behaviour change coincides with the development of infectivity of the parasite to the final host (a piscivorous bird), making it an ideal model for studying the mechanisms of infection-induced behavioural modification. However, whether the loss of host anti-predator behaviour results from direct manipulation by the parasite, or is a by-product (e.g. host immune response) or side effect of infection (e.g. energetic loss), remains controversial. To understand the physiological mechanisms that generate these behavioural changes, we quantified the behavioural profiles of experimentally infected fish and attempted to replicate these in non-parasitized fish by exposing them to treatments including immunity activation and fasting, or by pharmacologically inhibiting the stress axis. All fish were screened for the following behaviours: activity, water depth preference, sociability, phototaxis, anti-predator response and latency to feed. We were able to change individual behaviours with certain treatments. Our results suggest that the impact of S. solidus on the stickleback might be of a multifactorial nature. The behaviour changes observed in infected fish might result from the combined effects of modifying the serotonergic axis, lack of energy and activation of the immune system.

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“…It has been suggested that sticklebacks in populations with high infection pressure become locally adapted and are more resistant, i.e. have lower infection rates and more efficiently constrain S. solidus growth [17, 18]. On the other hand, S. solidus seems to adapt to the increased resistance of local hosts and become more virulent, i.e.…”

Section: Introductionmentioning

confidence: 99%

Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association

et al. 2017

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BackgroundIncreasing temperatures are predicted to strongly impact host-parasite interactions, but empirical tests are rare. Host species that are naturally exposed to a broad temperature spectrum offer the possibility to investigate the effects of elevated temperatures on hosts and parasites. Using three-spined sticklebacks, Gasterosteus aculeatus L., and tapeworms, Schistocephalus solidus (Müller, 1776), originating from a cold and a warm water site of a volcanic lake, we subjected sympatric and allopatric host-parasite combinations to cold and warm conditions in a fully crossed design. We predicted that warm temperatures would promote the development of the parasites, while the hosts might benefit from cooler temperatures. We further expected adaptations to the local temperature and mutual adaptations of local host-parasite pairs.ResultsOverall, S. solidus parasites grew faster at warm temperatures and stickleback hosts at cold temperatures. On a finer scale, we observed that parasites were able to exploit their hosts more efficiently at the parasite’s temperature of origin. In contrast, host tolerance towards parasite infection was higher when sticklebacks were infected with parasites at the parasite’s ‘foreign’ temperature. Cold-origin sticklebacks tended to grow faster and parasite infection induced a stronger immune response.ConclusionsOur results suggest that increasing environmental temperatures promote the parasite rather than the host and that host tolerance is dependent on the interaction between parasite infection and temperature. Sticklebacks might use tolerance mechanisms towards parasite infection in combination with their high plasticity towards temperature changes to cope with increasing parasite infection pressures and rising temperatures.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2192-7) contains supplementary material, which is available to authorized users.

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In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens

Cited by 29 publications

References 59 publications

Nematode infection in liver of the fish Gymnotus inaequilabiatus (Gymnotiformes: Gymnotidae) from the Pantanal Region in Brazil: pathobiology and inflammatory response

Nematode infection in liver of the fish Gymnotus inaequilabiatus (Gymnotiformes: Gymnotidae) from the Pantanal Region in Brazil: pathobiology and inflammatory response

Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?

Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association

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