Dataset Information

Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish.

ABSTRACT: Three different immunoglobulin (Ig) isotypes can be found in teleost fish, IgM, IgD, and the teleost-specific IgT. IgM is considered to have a systemic activity, and IgT is attributed a mucosal role, similar to mammalian IgA. In this study, the complete sequence of gilthead sea bream IgM and IgT in their membrane (m) and soluble (s) forms are described for the first time in a perciform fish. Their constitutive gene expression is analyzed in different tissues, and their regulation upon viral, bacterial, parasitic, mucosal vaccination and dietary challenges are studied. GCB IgM and IgT have the prototypical structure when compared to other fish Igs. The constitutive expression of sIgM was the highest overall in all tissues, whereas mIgT expression was highest in mucosal tissues, such as gills and intestine. IgM and IgT were differentially regulated upon infection. IgT was highly upregulated locally upon infection with the intestinal parasite Enteromyxum leei or systemically after Nodavirus infection. Long-term intestinal parasitic infections increased the serum titer of both isotypes. Mucosal vaccination against Photobacterium damselae subsp. piscicida finely regulated the Ig response inducing a systemic increase of IgM titers in serum and a local IgT response in skin mucus when animals were exposed to the pathogen by bath challenge. Interestingly, plant-based diets inhibit IgT upregulation upon intestinal parasitic challenge, which was related to a worse disease outcome. All these results corroborate the mucosal role of IgT and emphasize the importance of a finely tuned regulation of Ig isotypes upon infection, which could be of special interest in vaccination studies.

SUBMITTER: Piazzon MC

PROVIDER: S-EPMC5186763 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Publications

Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish.

Piazzon Maria C MC Galindo-Villegas Jorge J Pereiro Patricia P Estensoro Itziar I Calduch-Giner Josep A JA Gómez-Casado Eduardo E Novoa Beatriz B Mulero Victoriano V Sitjà-Bobadilla Ariadna A Pérez-Sánchez Jaume J

Frontiers in immunology 20161227

Three different immunoglobulin (Ig) isotypes can be found in teleost fish, IgM, IgD, and the teleost-specific IgT. IgM is considered to have a systemic activity, and IgT is attributed a mucosal role, similar to mammalian IgA. In this study, the complete sequence of gilthead sea bream IgM and IgT in their membrane (m) and soluble (s) forms are described for the first time in a perciform fish. Their constitutive gene expression is analyzed in different tissues, and their regulation upon viral, bac ...[more]

PMID: 28082977

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Project description:Upon infection, B-lymphocytes expressing antibodies specific for the intruding pathogen develop clonal responses triggered by pathogen recognition via the B-cell receptor. The constant region of antibodies produced by such responding clones dictates their functional properties. In teleost fish, the clonal structure of B-cell responses and the respective contribution of the three isotypes IgM, IgD and IgT remain unknown. The expression of IgM and IgT are mutually exclusive, leading to the existence of two B-cell subsets expressing either both IgM and IgD or only IgT. Here, we undertook a comprehensive analysis of the variable heavy chain (VH) domain repertoires of the IgM, IgD and IgT in spleen of homozygous isogenic rainbow trout (Onchorhynchus mykiss) before, and after challenge with a rhabdovirus, the Viral Hemorrhagic Septicemia Virus (VHSV), using CDR3-length spectratyping and pyrosequencing of immunoglobulin (Ig) transcripts. In healthy fish, we observed distinct repertoires for IgM, IgD and IgT, respectively, with a few amplified ? and ? junctions, suggesting the presence of IgM- and IgT-secreting cells in the spleen. In infected animals, we detected complex and highly diverse IgM responses involving all VH subgroups, and dominated by a few large public and private clones. A lower number of robust clonal responses involving only a few VH were detected for the mucosal IgT, indicating that both IgM(+) and IgT(+) spleen B cells responded to systemic infection but at different degrees. In contrast, the IgD response to the infection was faint. Although fish IgD and IgT present different structural features and evolutionary origin compared to mammalian IgD and IgA, respectively, their implication in the B-cell response evokes these mouse and human counterparts. Thus, it appears that the general properties of antibody responses were already in place in common ancestors of fish and mammals, and were globally conserved during evolution with possible functional convergences.

Project description:Many ecosystems are influenced simultaneously by multiple stressors. One important environmental stressor is aquatic pollution via wastewater treatment plant (WWTP) effluents. WWTP effluents may contribute to eutrophication or contain anthropogenic contaminants that directly and/or indirectly influence aquatic wildlife. Both eutrophication and exposure to anthropogenic contaminants may affect the dynamics of fish-parasite systems. With this in mind, we studied the impact of WWTP effluents on infection of brown trout by the parasite Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD). PKD is associated with the long-term decline of wild brown trout (Salmo trutta) populations in Switzerland. We investigated PKD infection of brown trout at two adjacent sites (?400 m apart) of a Swiss river. The sites are similar in terms of ecology except that one site receives WWTP effluents. We evaluated the hypothesis that fish inhabiting the effluent site will show greater susceptibility to PKD in terms of prevalence and disease outcome. We assessed susceptibility by (i) infection prevalence, (ii) parasite intensity, (iii) host health in terms of pathology, and (iv) estimated apparent survival rate. At different time points during the study, significant differences between sites concerning all measured parameters were found, thus providing evidence of the influence of effluents on parasitic infection of fish in our study system. However, from these findings we cannot determine if the effluent has a direct influence on the fish host via altering its ability to manage the parasite, or indirectly on the parasite or the invertebrate host via increasing bryozoa (the invertebrate host) reproduction. On a final note, the WWTP adhered to all national guidelines and the effluent only resulted in a minor water quality reduction assessed via standardized methods in this study. Thus, we provide evidence that even a subtle decrease in water quality, resulting in small-scale pollution can have consequences for wildlife.

Dataset Information

Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish.

Publications

Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish.

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