RNA-seq analysis of early enteromyxosis in turbot (Scophthalmus maximus): new insights into parasite invasion and immune evasion strategies

Ronza, Paolo; Robledo, Diego; Bermúdez, Roberto; Losada, Ana; Pardo, Belén G.; Sitjà‐Bobadilla, Ariadna; Quiroga, María Isabel; Martı́nez, Paulino

doi:10.1016/j.ijpara.2016.03.007

Cited by 48 publications

(56 citation statements)

References 81 publications

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“…Differential regulation of processes associated with both the innate and the adaptive immune system in immune organs and at the site of infection is a common feature in natural and experimental infections in vertebrates (e.g., Alvarez Rojas et al, 2015;Babayan et al, 2018;Huang et al, 2016) and the gradual shift from the regulation of innate to adaptive immune processes can be observed in gene expression studies (Ehret, Spork, Dieterich, Lucius, & Heitlinger, 2017). Additionally, parasite infections cause differential expression of genes not directly related to an immune response, such as those involved in metabolic processes, tissue repair, or organ function and development (Alvarez Rojas et al, 2015;Babayan et al, 2018;Ronza et al, 2016;Zhang et al, 2017) and this has also been observed in the European eel Schneebauer et al, 2017). How A. crassus affects gene expression in the Japanese eel and what processes are modified upon infection have not yet been determined for any parasitic stage.…”

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confidence: 99%

Gene expression response to a nematode parasite in novel and native eel hosts

Bracamonte

Johnston

Monaghan

et al. 2019

Ecology and Evolution

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Invasive parasites are involved in population declines of new host species worldwide. The high susceptibilities observed in many novel hosts have been attributed to the lack of protective immunity to the parasites which native hosts acquired during their shared evolution. We experimentally infected Japanese eels (Anguilla japonica) and European eels (Anguilla anguilla) with Anguillicola crassus, a nematode parasite that is native to the Japanese eel and invasive in the European eel. We inferred gene expression changes in head kidney tissue from both species, using RNA‐seq data to determine the responses at two time points during the early stages of infection (3 and 23 days postinfection). At both time points, the novel host modified the expression of a larger and functionally more diverse set of genes than the native host. Strikingly, the native host regulated immune gene expression only at the earlier time point and to a small extent while the novel host regulated these genes at both time points. A low number of differentially expressed immune genes, especially in the native host, suggest that a systemic immune response was of minor importance during the early stages of infection. Transcript abundance of genes involved in cell respiration was reduced in the novel host which may affect its ability to cope with harsh conditions and energetically demanding activities. The observed gene expression changes in response to a novel parasite that we observed in a fish follow a general pattern observed in amphibians and mammals, and suggest that the disruption of physiological processes, rather than the absence of an immediate immune response, is responsible for the higher susceptibility of the novel host.

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confidence: 99%

Gene expression response to a nematode parasite in novel and native eel hosts

Bracamonte

Johnston

Monaghan

et al. 2019

Ecology and Evolution

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“…Regulation of epithelial cell proliferation in response to macroparasite infections is associated with a pro‐inflammatory immune response in murine intestines (Cliffe et al., ) and in teleost skin (Kania, Evensen, Larsen, & Buchmann, ), involving cytokines such as TNFα and IL‐1β. Furthermore, studies relate regulation of epithelial cell proliferation to IFN‐γ production, which in turn modulates interleukin synthesis by macrophages (Artis, Potten, Else, Finkelman, & Grencis, ; Cliffe et al., ), and IFN‐related pathways were upregulated and played a main role at systemic as well as intestinal level during enteromyxosis in gilthead sea bream (Davey et al., ) and turbot (Ronza et al., ). Previous studies found a local shift towards an anti‐inflammatory cytokine response at 64 dpi (Pérez‐Cordón et al., ), supporting the gene expression reported for 113‐day chronic exposure (Sitjà‐Bobadilla et al., ).…”

Section: Discussionmentioning

confidence: 99%

Bromodeoxyuridine DNA labelling reveals host and parasite proliferation in a fish‐myxozoan model

Estensoro

Pérez-Cordón

Sitjà‐Bobadilla

et al. 2017

Journal of Fish Diseases

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Enteromyxum leei is a myxozoan parasite responsible for enteritis in gilthead sea bream (Sparus aurata). The parasite proliferates in the paracellular space of the intestinal epithelium and induces an inflammatory reaction. To assess intestinal cell turnover and parasite proliferation, fish were infected with the parasite by anal intubation; after 17 and 64 days, the cell proliferative marker bromodeoxyuridine (BrdU) was administered; and after 24 hr, tissue samples were taken for immunohistochemical detection. Parasite exposure induced increased epithelial and immune cell proliferation in all intestinal segments at all time points, even before parasite establishment. This increased turnover was triggered early after intubation and mainly at a local level, as shown by an increased proliferating cell nuclear antigen (pcna) gene expression only at the posterior intestine after 17 days (not found in lymphohaematopoietic organs). Incorporation of BrdU in parasite secondary and tertiary daughter cells indicated that parasite endogeny is not by schizogonial division, which uses de novo synthesis pathway of pyrimidines. Altogether, BrdU immunolabelling and pcna gene expression showed the rapid proliferative response of the fish intestines upon a myxozoan infection and how this response is effectively triggered even before the parasite reaches or establishes in the site.

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“…In gastrointestinal infections, direct alterations of the enteric nervous system also needs to be considered (Halliez & Buret 2015). In turbot Psetta maxima with entero myxosis, down-regulation of the neuropeptide Y-receptor NPY2R, a main regulator of appetite (Zou & Secombes 2011), has been reported in early stages of the infection (Ronza et al 2016). This observation is in agreement with the early onset of anorexia in Group A in the current trial, which was observed as early as 1 wk p.i.…”

Section: Discussionmentioning

confidence: 99%

Effect of a functional feed additive on mitigation of experimentally induced gilthead sea bream Sparus aurata enteromyxosis

et al. 2020

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In gilthead sea bream Sparus aurata, infection by Enteromyxum leei produces a cachectic syndrome with anorexia, weight loss, severe epaxial muscle atrophy and, eventually, death. Currently, there are neither vaccines nor effective prescription medicines to control this infection. Nutraceutical approaches are raising interest in the aquaculture industry, responding to the lack of therapeutic tools for the management of insidious chronic losses due to parasites. In this study, the effect of a commercially available health-promoting feed additive (SANACORE ® GM) at 2 different doses was tested in comparison with a basal diet without the additive during a laboratory-controlled challenge with E. leei. Group performance and biometrical values were monitored, and an in-depth parasitological diagnosis, quantification of parasite loads and histopathological examination were carried out at the end of the trial. Supplemented diets mitigated the anorexia and growth arrestment observed in challenged fish fed the basal diet. This mitigation was maximum in the highest dose group, whose growth performance was not different from that of unchallenged controls. Treated groups also presented lower prevalence of infection and a lower parasite load, although the differences in the mean intensity of infection were not statistically significant. Although the decrease in parasite levels was similar with both doses of additive tested, the pathogeny of the infection was mostly suppressed with the higher dose, while only mitigated with the lower dose. The mechanisms involved in the effects obtained remain to be investigated, but the results point to a modulation of the immunopathological response to the infection.

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RNA-seq analysis of early enteromyxosis in turbot (Scophthalmus maximus): new insights into parasite invasion and immune evasion strategies

Abstract: 27Enteromyxum scophthalmi, an intestinal myxozoan parasite, is the causative agent of a

Cited by 48 publications

References 81 publications

Gene expression response to a nematode parasite in novel and native eel hosts

Gene expression response to a nematode parasite in novel and native eel hosts

Bromodeoxyuridine DNA labelling reveals host and parasite proliferation in a fish‐myxozoan model

Effect of a functional feed additive on mitigation of experimentally induced gilthead sea bream Sparus aurata enteromyxosis

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