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.
Highlights
In teleost fish, three different immunoglobulin (Ig) isotypes are found, IgM, IgD, and the teleost-specific IgT which originated from a duplication of the Cμ [1,2,3]
IgT has been initially proposed to have its main role in mucosal immunity, being the functional equivalent in teleosts of mammalian IgA [4, 5], but later studies have shown that the involvement of IgT in the immune response might not be restricted to the mucosal tissues, and the humoral response of teleosts is more complex than initially predicted [6]
The data mining revealed the presence of full length sequences for both, soluble (s) and membrane (m) bound, heavy chains of IgM and IgT, which were uploaded to GenBank with the following accession numbers: sigm JQ811851, mIgM KX599199, sIgT KX599200, and mIgT KX599201
Summary
Three different immunoglobulin (Ig) isotypes are found, IgM, IgD, and the teleost-specific IgT which originated from a duplication of the Cμ [1,2,3]. IgT, named IgZ, was first described in 2005 in rainbow trout [2] and zebrafish [1], the two different nomenclatures. The latest trend is to use the term IgT to refer to this teleost-specific isotype. Histochemical studies in rainbow trout intestine revealed that IgM+ B cells appear preferentially in the lamina propria and IgT+ cells in the epithelium [7], showing a clear physical compartmentalization of these different B cell types. The same study showed that oral vaccination against infectious pancreatic necrosis virus (IPNV) induced an increase in both IgT+ and IgM+ cells, indicating that both cell types are important for mucosal responses. IgT, despite being generally less abundant than IgM in number of transcripts and cells, is undeniably crucial in mucosal immune responses, but its role in systemic responses [13, 14] and the role of IgM in mucosal responses should not be discarded
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