Prevailing Role of Mucosal Igs and B Cells in Teleost Skin Immune Responses to Bacterial Infection

Abstract

The skin of vertebrates is the outermost organ of the body and serves as the first line of defense against external aggressions. In contrast to mammalian skin, that of teleost fish lacks keratinization and has evolved to operate as a mucosal surface containing a skin-associated lymphoid tissue (SALT). Thus far, IgT representing the prevalent immunoglobulin (Ig) in SALT have only been reported upon infection with a parasite. However, very little is known about the types of B cells and Igs responding to bacterial infection in the teleost skin mucosa, as well as the inductive or effector role of the SALT in such responses. To address these questions, here we analyzed the immune response of trout skin upon infection with one of the most widespread fish skin bacterial pathogens, Flavobacterium columnare. This pathogen induced strong skin innate immune and inflammatory responses at the initial phases of infection. More critically, we found that the skin mucus of fish having survived the infection contained significant IgT-but not IgM-or IgD-specific titers against the bacteria. Moreover, we demonstrate the local proliferation and production of IgT + B-cells and specific IgT titers respectively within the SALT upon bacterial infection. Thus, our findings represent the first demonstration that IgT is the main Ig isotype induced by the skin mucosa upon bacterial infection, and that because of the large surface of the skin, its SALT probably represents a prominent IgT inductive site in fish..

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses

“…Given the lack of lymph nodes containing germinal centers (GCs) in teleost fish, it is unclear whether the accumulation of IgT + B-cells observed in the SB mucosa is the result of local B-cell proliferation or migration from other lymphoid organs. Here, we found significant proliferative IgT + B-cell responses in the SB mucosa of trout after infection with IHNV, similar to what we have previously been reported in other fish mucosa infected with different pathogens 25 , 26 . Moreover, we detected strong IgM + and moderate IgT + B-cell proliferative responses in the HK of the same fish.…”

“…Teleost fish represent the oldest bony vertebrates featuring MALT and bonafide immunoglobulins (Igs) 20 – 22 . Breaking the old paradigm that mucosal Igs were present only in tetrapod species, we have previously shown that teleosts contain IgT, the most ancient Ig specialized in mucosal immunity against parasitic and bacterial pathogens 23 – 25 . Moreover, we have demonstrated that, analogously to mammalian IgA, teleost secretory IgT (sIgT) is the main sIg isotype coating the microbiota of mucosal surfaces.…”

Commensal bacteria‐immunity crosstalk shapes mucosal homeostasis in teleost fish

“…Recently, studies demonstrated that Flavobacterium columnare could induce the proliferation of IgT + B cells in the skin and buccal mucosa of rainbow trout, and also induces dominant IgT-specific responses in the skin and buccal mucus, and IgM-specific responses in serum of rainbow trout, respectively. 180,230 Similarly, specific Igs responses to Flavobacterium columnare were detected in gills and nasal mucus of rainbow trout upon immersion challenge (Figure 2). 231,232 These results demonstrate that opportunistic pathogens could elicit mucosal and system-specific Igs responses, and such specific immune responses might prevent the pathogen from re-infection.…”

“…NALT, buccal mucosa and pharyngeal mucosa) is poorly understood. Recently, studies demonstrated that Flavobacterium columnare could induce the proliferation of IgT + B cells in the skin and buccal mucosa of rainbow trout, and also induces dominant IgT‐specific responses in the skin and buccal mucus, and IgM‐specific responses in serum of rainbow trout, respectively 180,230 . Similarly, specific Igs responses to Flavobacterium columnare were detected in gills and nasal mucus of rainbow trout upon immersion challenge (Figure 2).…”

Fructose Promotes Crucian Carp Survival Against Aeromonas hydrophila Infection

“…Meanwhile, the exploration of cell-mediated immune and antibody-dependent clearance of bacterial pathogens also sheds light on novel targets to treat bacterial infections ( 39 – 42 ). For example, IgT emerged as a key factor in defending against bacterial pathogens, which are present in the mucosa of teleost fish ( 43 ).…”