Mucosal immunoglobulins and B cells of teleost fish

Abstract

As physical barriers that separate teleost fish from the external environment, mucosae are also active immunological sites that protect them against exposure to microbes and stressors. In mammals, the sites where antigens are sampled from mucosal surfaces and where stimulation of naive T and B lymphocytes occurs are known as inductive sites and are constituted by mucosa-associated lymphoid tissue (MALT). According to anatomical location, the MALT in teleost fish is subdivided into gut-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), and gill-associated lymphoid tissue (GIALT). All MALT contain a variety of leukocytes, including, but not limited to, T cells, B cells, plasma cells, macrophages and granulocytes. Secretory immunoglobulins are produced mainly by plasmablasts and plasma cells, and play key roles in the maintenance of mucosal homeostasis. Until recently, teleost fish B cells were thought to express only two classes of immunoglobulins, IgM and IgD, in which IgM was thought to be the only one responding to pathogens both in systemic and mucosal compartments. However, a third teleost immunoglobulin class, IgT/IgZ, was discovered in 2005, and it has recently been shown to behave as the prevalent immunoglobulin in gut mucosal immune responses. The purpose of this review is to summarise the current knowledge of mucosal immunoglobulins and B cells of fish MALT. Moreover, we attempt to integrate the existing knowledge on both basic and applied research findings on fish mucosal immune responses, with the goal to provide new directions that may facilitate the development of novel vaccination strategies that stimulate not only systemic, but also mucosal immunity.

Teleost skin, an ancient mucosal surface that elicits gut-like immune responses

“…In addition, the mammalian SALT includes also the skin-draining lymph nodes where induction of immunity occurs by antigens that have been processed and transported by LCs. Thus far, very little is known about the components of the teleost SALT although it has been reported to contain secretory cells that produce mucus (i.e., goblet cells), lymphocytes, granulocytes, macrophages, and Langerhans-like cells (3,12,13). Because the skin of fish lacks keratinization and is coated by a mucosal layer and because fish don't contain organized lymphoid structures, the teleost SALT cannot be considered a counterpart of that of mammals.…”

“…Teleost IgM is by far the most prevalent Ig in plasma and is the principal Ig involved in systemic immunity although it has also been shown to be involved in mucosal responses (3). In that regard, antigenspecific IgM, albeit low, has been demonstrated in teleost gut and skin mucus (3). Although secreted IgD has been identified in the plasma of teleost species (6), its function remains unknown.…”

“…Only three Ig classes: IgM, IgD, and IgT/Z have been identified thus far in teleosts (3). Teleost IgM is by far the most prevalent Ig in plasma and is the principal Ig involved in systemic immunity although it has also been shown to be involved in mucosal responses (3). In that regard, antigenspecific IgM, albeit low, has been demonstrated in teleost gut and skin mucus (3).…”

“…Therefore, it would appear that the histological differences seen in the skin of vertebrates (i.e., scales, feathers, or hair, and secretion of mucus or sweat) are mainly the result of their adaptation into watercontaining or dry-land environments. Interestingly, early vertebrates like fish originated in aquatic environments, and therefore their skin behaves as a mucosal surface that harbors abundant mucus-producing cells, lacks keratinization, and possesses living epithelial cells in direct contact with the water medium (3). When vertebrates colonized the land, their skin underwent important evolutionary changes, including loss of mucus production, acquisition of dead keratinized cell layers, and other adaptations such as hair follicles and sweat glands in the case of mammals (1).…”

Development of an Ussuri catfish Pseudobagrus ussuriensis skin cell line displaying differential cytopathic effects to three aquatic animal viruses

“…In addition, cell lines derived from catfish were also rare. Fish skin, as the primary interface between the body and the water environment, may participate in a series of physiological reactions and provide an important barrier against microbial pathogens (Zhao et al, 2008;Tsutsui et al, 2009;Salinas et al, 2011). The cell line derived from skin of Ussuri catfish would be helpful for studying the pathology and physiology of this species.…”