CCR7 Is Mainly Expressed in Teleost Gills, Where It Defines an IgD+IgM− B Lymphocyte Subset

Abstract

Chemokine receptor CCR7, the receptor for both CCL19 and CCL21 chemokines, regulates the recruitment and clustering of circulating leukocytes to secondary lymphoid tissues, such as lymph nodes and Peyer's patches. Even though teleost fish do not have either of these secondary lymphoid structures, we have recently reported a homolog to CCR7 in rainbow trout (Oncorhynchus mykiss). In the present work, we have studied the distribution of leukocytes bearing extracellular CCR7 in naive adult tissues by flow cytometry, observing that among the different leukocyte populations, the highest numbers of cells with membrane (mem)CCR7 were recorded in the gill (7.5 ± 2% CCR7+ cells). In comparison, head kidney, spleen, thymus, intestine, and peripheral blood possessed <5% CCR7+ cells. When CCR7 was studied at early developmental stages, we detected a progressive increase in gene expression and protein CCR7 levels in the gills throughout development. Surprisingly, the majority of the CCR7+ cells in the gills were not myeloid cells and did not express membrane CD8, IgM, nor IgT, but expressed IgD on the cell surface. In fact, most IgD+ cells in the gills expressed CCR7. Intriguingly, the IgD+CCR7+ population did not coexpress memIgM. Finally, when trout were bath challenged with viral hemorrhagic septicemia virus, the number of CCR7+ cells significantly decreased in the gills while significantly increased in head kidney. These results provide evidence of the presence of a novel memIgD+memIgM− B lymphocyte subset in trout that expresses memCCR7 and responds to viral infections. Similarities with IgD+IgM− subsets in mammals are discussed.

Transcriptional Characterization of the T Cell Population within the Salmonid Interbranchial Lymphoid Tissue

“…The ILT responds to infection in a different manner compared with the other tissues examined, especially noteworthy the gills, in which the ILT is located. The gills as a mucosal tissue have previously been hypothesized as the location of less evolved lymphoid organizations in teleosts (6). The strategic location of the ILT gives the mucosal immune system a unique possibility of an early onset of local immune mechanisms right at the border to the external environment, a location that under no doubt is subjected to considerable exposure of both unharmful commensal microorganisms and Ags presenting a threat to the organism.…”

“…The presence of peaceful coexistence with commensals depends on mechanisms that limit the initiation of immune responses unless strictly required, similar to that found in lungs of humans (46). Similarly, clonal anergy of B cells might represent another surveillance system in the gills (6). The extraordinary heterogeneous population of T cells located within the ILT contributes beyond doubt to the local immune defense in the gills, and future studies will aim to reveal the mechanisms by which the ILT exerts its function.…”

“…Seeing that the thymus and the ILT develop from the same area, it is highly plausible that they share joint functions. The identification of thymus-like lymphoepithelial structures termed thymoids, located in gill tips and secondary lamellae of lamprey larvae (5) has further sparked interest into exciting investigations of lymphoid organizations in gills of teleosts (6).…”

Physiology and immunology of mucosal barriers in catfish (Ictalurus spp.)

“…There has been a study using rainbow trout that characterized a similar B-cell subset (IgM-/IgDC/CCR7C) that is predominantly found in the gill and undergoes migration to the head kidney during a viral infection. 115 We don't currently have a complete view on how the mucosal adaptive immune system operates in teleost fish. It would be of interest to investigate B-cell lineage development at the mucosal sites in response to antigen both under normal and disease conditions, including clarifying the nature of expected mucosal Ig isotypes in channel catfish.…”

Identification of Teleost Skin CD8α+ Dendritic-like Cells, Representing a Potential Common Ancestor for Mammalian Cross-Presenting Dendritic Cells

“…The anti-trout CD8a (mAb rat IgG; 7 mg/ml) and the anti-trout CCR7 (pAb rabbit IgG; 2 mg/ml) used in this study were characterized previously (34,35). The anti-trout MHC class II b-chain (mAb mouse IgG1; 2 mg/ml) was characterized above.…”