Abstract
In mammals, M cells can take up antigens through mucosal surfaces of the gut and the respiratory tract. Since M cells are deficient of lysosomes and phagosomes, the antigens are directly delivered to the mucosa-associated lymphoid tissue (MALT) without degradation. In teleost fish, the entire body surface (gills, skin, and intestinal system) is covered by mucus; however, specific antigen-sampling cells have not yet been identified in their mucosal tissues. Here, we show that two phenotypes of antigen-sampling cells take up antigens through epithelial surfaces of the rainbow trout gill. One phenotype of antigen-sampling cells has features of monocyte/macrophage/dendritic cell-type cells; they have large vacuoles in the cytoplasm and express PTPRC (CD45), CD83, IL-1β, and IL-12p40b. The second phenotype exhibits similar characteristics to mammalian M cells; the corresponding cells bind the lectin UEA-1 but not WGA and show expression of M cell marker gene Anxa5. In contrast to mammalian M cells, teleost M-type cells were found to exhibit small vacuoles in their cytoplasm and to express almost all genes related to the “phagosome”, “lysosome,” and “antigen processing and presentation” pathways. Furthermore, MHC class II was constitutively expressed on a fraction of M-type cells, and this expression was significantly increased after antigen uptake, suggesting that the MHC class II is inducible by antigen stimulation. Here, we suggest that teleost M-type cells play a role in the phylogenetically primitive teleost immune system, similar to bona-fide M cells. In addition, the presence of MHC class II expression suggests an additional role in antigen presentation in the gills, which are an organ with high T cell abundance, especially in interbranchial lymphoid tissue. The present results suggest an unconventional antigen presentation mechanism in the primitive mucosal immune system of teleosts, which generally lack highly organized lymphoid tissues. Moreover, the results of this work may be valuable for the development of mucosal vaccines that specifically target M-type cells; mucosal vaccines significantly reduce working costs and the stress that is usually induced by vaccination via injection of individual fish.
Highlights
The mucosal surfaces of the digestive and respiratory systems are continuously exposed to the external environment and represent potential ports of pathogen entry
Double staining with an antiAss polyclonal antibody and either of the lectins after bath vaccination revealed that both Ulex europaeus agglutinin-1 (UEA-1)+ and UEA-1− cells were able to take up Ass bacterin (Figure 1C), while wheat germ agglutinin (WGA)+ cells were not (Figure 1D)
We identified two cell populations that take up bacterins in the gill epithelium of bath-vaccinated rainbow trout
Summary
The mucosal surfaces of the digestive and respiratory systems are continuously exposed to the external environment and represent potential ports of pathogen entry. Molecules on the surface of M cells such as glycoprotein 2 [4], integrin β1 [5], and α2-3-linked sialic acid [6] have been identified as receptors involved in the uptake of FimH+ bacteria, Yersinia enterocolitica and type 1 reovirus, respectively. Following their capture by the corresponding receptors, M cells mainly transcytose the respective antigens and deliver them to subjacent APCs [7], and the APCs present antigens to T lymphocytes in MALT. Antigen-specific immune responses, such as production of IgA by B cells, are induced in mucosal tissues
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