The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens

Abstract

The field of mucosal immunology research has grown fast over the past few years, and our understanding on how mucosal surfaces respond to complex antigenic cocktails is expanding tremendously. With the advent of new molecular sequencing techniques, it is easier to understand how the immune system of vertebrates is, to a great extent, orchestrated by the complex microbial communities that live in symbiosis with their hosts. The commensal microbiota is now seen as the "extended self" by many scientists. Similarly, fish immunologist are devoting important research efforts to the field of mucosal immunity and commensals. Recent breakthroughs on our understanding of mucosal immune responses in teleost fish open up the potential of teleosts as animal research models for the study of human mucosal diseases. Additionally, this new knowledge places immunologists in a better position to specifically target the fish mucosal immune system while rationally designing mucosal vaccines and other immunotherapies. In this review, an updated view on how teleost skin, gills and gut immune cells and molecules, function in response to pathogens and commensals is provided. Finally, some of the future avenues that the field of fish mucosal immunity may follow in the next years are highlighted.

Keywords: Commensal; Immune system; Mucosa; Pathogen; Teleost.

Fig. 1

Esquematic representation of the similarities and differences between teleost fish skin, gills and gut, and mammalian skin and type I mucosal surfaces. Structural differences in the type and number of layers of epithelial cells, as well as the presence of keratine or mucus (and mucus producing cells) are displayed in the upper half of each diagram. In the bottom the connective tissue, named dermis in skin and lamina propria in gut and gills, is exhibited. Similarities in the celular components of the innate immune system (Langerhans cells, dendritic cells, macrophages, granulocytes and mast cells) are also displayed. Differences in the localization of B and T cells, the isotype of immunoglobulins and the prescence of the secretory component (SC) of the polymeric immonoglobulin receptor (pIgR) are represented as well. Finally, the presence of commensal bacteria and antimicrobial peptides (AMPs) is shown in the outer mucosal surface or over the keratin layer. Elements that are suspected to be present in a tissue, but have not been studied so far are marked as unknown (?).