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

Yong-Yao Yu,Irene Salinas,Zhen-Yu Huang,Guang-Mei Yin,Zhen Xu,Fen Dong,Yong-An Zhang,Ya-Xing Yin,Shuai Dong,Weiguang Kong,Daniel R Barreda

doi:10.1371/journal.ppat.1007251

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.

Highlights

Olfaction is a vital sense for all animals [1]
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
We found that a portion of IgT in the nasal mucosa was present in polymeric form, as it eluted at a fraction similar to that of trout nasal IgM, a tetrameric Ig (Fig 1A), and simultaneously, some IgT was consistently eluted in monomeric form

Summary

Introduction

To receive an olfactory signal, terrestrial vertebrates inhale gases containing volatile chemical substances, while aquatic vertebrates like teleost fish actively draw water containing dissolved chemicals into the olfactory organs [2]. During this process, the olfactory organs are constantly stimulated by toxins and pathogens in the air or water [3]. Similar to the Peyer’s patches in the guts of mammals, O-NALT has distinct B-cell zones [5, 6], and humoral immune responses occur in response to infection or antigenic stimulation [7]. From an evolutionary viewpoint, NALT in teleost fish is equipped to rapidly respond to antigens present in the water environment [3]

Methods

Results

Conclusion