Mucosal immunoglobulins protect the olfactory organ of teleost fish against parasitic infection

Abstract

The olfactory organ of vertebrates receives chemical cues present in the air or water and, at the same time, they are exposed to invading pathogens. Nasal-associated lymphoid tissue (NALT), which serves as a mucosal inductive site for humoral immune responses against antigen stimulation in mammals, is present also in teleosts. IgT in teleosts is responsible for similar functions to those carried out by IgA in mammals. Moreover, teleost NALT is known to contain B-cells and teleost nasal mucus contains immunoglobulins (Igs). Yet, whether nasal B cells and Igs respond to infection remains unknown. We hypothesized that water-borne parasites can invade the nasal cavity of fish and elicit local specific immune responses. To address this hypothesis, we developed a model of bath infection with the Ichthyophthirius multifiliis (Ich) parasite in rainbow trout, Oncorhynchus mykiss, an ancient bony fish, and investigated the nasal adaptive immune response against this parasite. Critically, we found that Ich parasites in water could reach the nasal cavity and successfully invade the nasal mucosa. Moreover, strong parasite-specific IgT responses were detected in the nasal mucus, and the accumulation of IgT+ B-cells was noted in the nasal epidermis after Ich infection. Strikingly, local IgT+ B-cell proliferation and parasite-specific IgT generation were found in the trout olfactory organ, providing new evidence that nasal-specific immune responses were induced locally by a parasitic challenge. Overall, our findings suggest that nasal mucosal adaptive immune responses are similar to those reported in other fish mucosal sites and that an antibody system with a dedicated mucosal Ig performs evolutionary conserved functions across vertebrate mucosal surfaces.

Review on Immersion Vaccines for Fish: An Update 2019

“…Immune cells are present in all mucosal tissues/linings (MALT), from nasopharynx-associated lymphoid tissue (NALT), gill-associated lymphoid tissue (GIALT), skin-associated lymphoid tissue (SALT), buccal cavity-associated lymphoid tissue, and gut-associated lymphoid tissue (GALT). These tissues contain characteristics important to the adaptive immune system [28][29][30][31][32][33]. The mucosal integument and soft tissues also contain innate defense molecules which may be fully protective against early stage infection [34].…”

Viral-Infected Change of the Digestive Tract Microbiota Associated With Mucosal Immunity in Teleost Fish

“…After dissected and fixed in 4% neutral buffered formalin at 4 • C, the mouth, pharynx, stomach, foregut, midgut, and hindgut of the trout were then dehydrated in a graded ethanol series, cleaned in xylene, embedded in paraffin, and cut in sections of 5 µm in duplicate with a rotary microtome (MICROM International GmbH, Germany). A copy of the sections were stained with classical hematoxylin and eosin (H & E) and alcian blue (A & B) as described previously (15,16). Images were acquired in microscope (Olympus, Japan) using the Axiovision software.…”

Pharyngeal Immunity in Early Vertebrates Provides Functional and Evolutionary Insight into Mucosal Homeostasis

“…Although organized NALT structures in sarcopterygian fish like lungfish are found in the mucosa of the upper and lower jaw, they still lack B and T cell zones and GC formation (16). It is worth noting that teleost NALT has only been described as diffuse NALT in the NC, and it shares the main features of other teleost MALTs, including a dominant role of secreted IgT (sIgT) and IgT + B cells in mucosal immunity (17,18). However, because teleost fish lack the choana, and the PC is a separate compartment from the NC, whether MALT appears in the teleost PC remains an enigmatic question.…”