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The right response at the right time: Exploring helminth immune modulation in sticklebacks by experimental coinfection.

ABSTRACT: Parasites are one of the strongest selective agents in nature. They select for hosts that evolve counter-adaptive strategies to cope with infection. Helminth parasites are special because they can modulate their hosts' immune responses. This phenomenon is important in epidemiological contexts, where coinfections may be affected. How different types of hosts and helminths interact with each other is insufficiently investigated. We used the three-spined stickleback (Gasterosteus aculeatus) - Schistocephalus solidus model to study mechanisms and temporal components of helminth immune modulation. Sticklebacks from two contrasting populations with either high resistance (HR) or low resistance (LR) against S. solidus, were individually exposed to S. solidus strains with characteristically high growth (HG) or low growth (LG) in G. aculeatus. We determined the susceptibility to another parasite, the eye fluke Diplostomum pseudospathaceum, and the expression of 23 key immune genes at three time points after S. solidus infection. D. pseudospathaceum infection rates and the gene expression responses depended on host and S. solidus type and changed over time. Whereas the effect of S. solidus type was not significant after three weeks, T regulatory responses and complement components were upregulated at later time points if hosts were infected with HG S. solidus. HR hosts showed a well orchestrated immune response, which was absent in LR hosts. Our results emphasize the role of regulatory T cells and the timing of specific immune responses during helminth infections. This study elucidates the importance to consider different coevolutionary trajectories and ecologies when studying host-parasite interactions.

SUBMITTER: Piecyk A

PROVIDER: S-EPMC6852435 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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The right response at the right time: Exploring helminth immune modulation in sticklebacks by experimental coinfection.

Piecyk Agnes A Ritter Marc M Kalbe Martin M

Molecular ecology 20190517 10

Parasites are one of the strongest selective agents in nature. They select for hosts that evolve counter-adaptive strategies to cope with infection. Helminth parasites are special because they can modulate their hosts' immune responses. This phenomenon is important in epidemiological contexts, where coinfections may be affected. How different types of hosts and helminths interact with each other is insufficiently investigated. We used the three-spined stickleback (Gasterosteus aculeatus) - Schis ...[more]

PMID: 30993799

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Project description:BackgroundAscariasis and malaria are highly prevalent parasitic diseases in tropical regions and often have overlapping endemic areas, contributing to high morbidity and mortality rates in areas with poor sanitary conditions. Several studies have previously aimed to correlate the effects of Ascaris-Plasmodium coinfections but have obtained contradictory and inconclusive results. Therefore, the present study aimed to investigate parasitological and immunopathological aspects of the lung during murine experimental concomitant coinfection by Plasmodium berghei and Ascaris suum during larvae ascariasis.MethodsC57BL/6J mice were inoculated with 1 × 104 P. berghei strain NK65-NY-infected red blood cells (iRBCs) intraperitoneally and/or 2500 embryonated eggs of A. suum by oral gavage. P. berghei parasitaemia, morbidity and the survival rate were assessed. On the seventh day postinfection (dpi), A. suum lung burden analysis; bronchoalveolar lavage (BAL); histopathology; NAG, MPO and EPO activity measurements; haematological analysis; and respiratory mechanics analysis were performed. The concentrations of interleukin (IL)-1β, IL-12/IL-23p40, IL-6, IL-4, IL-33, IL-13, IL-5, IL-10, IL-17A, IFN-γ, TNF and TGF-β were assayed by sandwich ELISA.ResultsAnimals coinfected with P. berghei and A. suum show decreased production of type 1, 2, and 17 and regulatory cytokines; low leukocyte recruitment in the tissue; increased cellularity in the circulation; and low levels of NAG, MPO and EPO activity that lead to an increase in larvae migration, as shown by the decrease in larvae recovered in the lung parenchyma and increase in larvae recovered in the airway. This situation leads to severe airway haemorrhage and, consequently, an impairment respiratory function that leads to high morbidity and early mortality.ConclusionsThis study demonstrates that the Ascaris-Plasmodium interaction is harmful to the host and suggests that this coinfection may potentiate Ascaris-associated pathology by dampening the Ascaris-specific immune response, resulting in the early death of affected animals.

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The right response at the right time: Exploring helminth immune modulation in sticklebacks by experimental coinfection.

Publications

The right response at the right time: Exploring helminth immune modulation in sticklebacks by experimental coinfection.

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