IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon

Abstract

B cells of teleost fish differentiate in the head kidney, and spleen, and either remain in the lymphatic organs or move to the blood and peripheral tissues. There is limited knowledge about piscine B cell traffic to sites of vaccination and infection and their functional roles at these sites. In this work, we examined the traffic of B cells in Atlantic salmon challenged with salmonid alphavirus (SAV). In situ hybridization (RNAScope) showed increased numbers of immunoglobin (Ig)M+ and IgT+ B cells in the heart in response to SAV challenge, with IgM+ B cells being most abundant. An increase in IgT+ B cells was also evident, indicating a role of IgT+ B cells in nonmucosal tissues and systemic viral infections. After infection, B cells were mainly found in the stratum spongiosum of the cardiac ventricle, colocalizing with virus-infected myocardial-like cells. From sequencing the variable region of IgM in the main target organ (heart) and comparing it with a major lymphatic organ (the spleen), co-occurrence in antibody repertoires indicated a transfer of B cells from the spleen to the heart, as well as earlier recruitment of B cells to the heart in vaccinated fish compared to those that were unvaccinated. Transcriptome analyses performed at 21 days post-challenge suggested higher expression of multiple mediators of inflammation and lymphocyte-specific genes in unvaccinated compared to vaccinated fish, in parallel with a massive suppression of genes involved in heart contraction, metabolism, and development of tissue. The adaptive responses to SAV in vaccinated salmon appeared to alleviate the disease. Altogether, these results suggest that migration of B cells from lymphatic organs to sites of infection is an important part of the adaptive immune response of Atlantic salmon to SAV.

Monoclonal antibody generated against Nile tilapia (Oreochromis niloticus) IgT heavy chain using a peptide-based strategy

“…The IgT + B cells comprise a separate lineage of fish B cells that appears to have a main role in mucosal surfaces such as the gut, the skin and the gills [ 13 , 15 , 19 ], and only has being extensively characterized in rainbow trout and zebrafish ( Danio rerio ) [ 4 , 10 , 18 , 21 ]. Other studies conducted in sea bass ( Dicentrarchus labrax ) [ 8 , 9 ], Atlantic salmon [ 55 , 56 ], large yellow croaker ( Larimichthys crocea ) [11] and grouper ( Epinephelus coioides ) [12] shed light over some aspects of the structural and functional characteristics of this Ig isotype. The present study describes for the first time the use of a monoclonal antibody against Nile tilapia IgT in the identification of IgT + B lymphocyte populations by flow cytometry.…”

“…Upon activation, B cells start a differentiation process that leads them to a plasmablast state, and they eventually to become plasma cells, with a greater capacity to secrete immunoglobulins (Igs) [57] . The IgT has been described as an Ig specialized in mucosal immunity [13] , but some studies reported the presence and activation of IgT + B cells in systemic compartments after viral, bacterial or parasitic challenge [ 3 , 10 , 56 , 58 ]. The effect of the enteric myxozoan parasite Enteromyxum leei on circulating Igs in gilthead sea bream ( Sparus aurata ) from a long-term infection revealed a significant increase in IgT levels in serum, which was significantly higher than IgM levels in challenged fish.…”

Identification and characterization of immunoglobulin tau (IgT) in Asian Seabass (Lates calcarifer) and mucosal immune response to nervous necrosis virus

“…IgT found in the MALTs is known to coat mucosal pathogens and microbiota, particularly in the gut and gill to maintain mucosal homeostasis ( 12 ). Additionally, IgT + B cells have been observed to be mobilized to the infection site in-vivo ( 13 ).…”

Evaluation of Immune Status in Two Cohorts of Atlantic Salmon Raised in Different Aquaculture Systems (Case Study)

“…NSAB can be detected in the assay by binding circulating antibodies to model antigens toward which the Atlantic salmon has never been exposed. Our recent studies showed strong responses of NSAB to vaccination, functional disorders and infections with pathogens indicating their importance in Atlantic salmon [13][14][15][16]. Sequencing of the variable region of IgM heavy chain (Ig-seq) evaluates the size and complexity of the antibody repertoire [17].…”

“…Each unique sequence (clonotype) serves as a barcode for clonal B cells derived from a single progenitor cell. The sharing of identical clonotypes between tissues reflects a migration of B cells [15].…”