RNA-seq analysis reveals significant transcriptome changes in turbot (Scophthalmus maximus) suffering severe enteromyxosis

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

doi:10.1186/1471-2164-15-1149

Cited by 64 publications

(87 citation statements)

References 96 publications

(116 reference statements)

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“…The European eel was previously shown to produce antibodies against adult A. crassus (Knopf & Lucius, ; Nielsen, ), thus the presence of adult parasites may enhance the immune response, as discussed above for the Japanese eel. Second, the response to an infection differs among organs (Bracamonte et al, ; Huang et al, ; Robledo et al, ). If an immune response is induced locally but not systemically, it would only be detectable in the infected organ.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…Interestingly, survivor fish (around 4 months post infection) appear to be protected against a secondary infection with E. scophthalmi due to some innate parameters, but mainly by the presence of specific antibodies (Sitjà-Bobadilla et al, 2007). In a recent study in turbot infected with high doses of E. scophthalmi , RNA-seq showed an increase in Ig-related genes in the pyloric caeca region 42 days post oral infection (Robledo et al, 2014), corroborating the late importance of B cells in parasite infection.…”

Section: Mucosal B Cell Responses In Gutmentioning

confidence: 81%

B cells and their role in the teleost gut

Parra

Korytář

Takizawa

et al. 2016

Developmental & Comparative Immunology

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Mucosal surfaces are the main route of entry for pathogens in all living organisms. In the case of teleost fish, mucosal surfaces cover the vast majority of the animal. As these surfaces are in constant contact with the environment, fish are perpetually exposed to a vast number of pathogens. Despite the potential prevalence and variety of pathogens, mucosal surfaces are primarily populated by commensal non-pathogenic bacteria. Indeed, a fine balance between these two populations of microorganisms is crucial for animal survival. This equilibrium, controlled by the mucosal immune system, maintains homeostasis at mucosal tissues. Teleost fish possess a diffuse mucosa-associated immune system in the intestine, with B cells being one of the main responders. Immunoglobulins produced by these lymphocytes are a critical line of defense against pathogens and also prevent the entrance of commensal bacteria into the epithelium. In this review we will summarize recent literature regarding the role of B-lymphocytes and immunoglobulins in gut immunity in teleost fish, with specific focus on immunoglobulin isotypes and the microorganisms, pathogenic and non-pathogenic that interact with the immune system.

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“…Turbot enteromyxosis ends up in lethal catarrhal enteritis, and the parasite is much more pathogenic in this host than E. leei in gilthead sea bream. Transcriptomic analyses of turbot enteromyxosis revealed a complex cell death/proliferation balance, but in the pyloric caeca of infected turbot, tissue repair and cell proliferation genes (including pcna ) were significantly upregulated (Robledo et al., ). Similarly, a complex interplay between host‐ and/or parasite‐mediated apoptosis and cell proliferation was reported for the gene expression in E. leei ‐infected PI of gilthead sea bream, in which the regenerative action was evidenced by the upregulation of genes involved in cell proliferation (Calduch‐Giner et al., ; Davey 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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RNA-seq analysis reveals significant transcriptome changes in turbot (Scophthalmus maximus) suffering severe enteromyxosis

Cited by 64 publications

References 96 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

B cells and their role in the teleost gut

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

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