Discovery of an organized nasopharynx-associated lymphoid tissue in the nasal cavity of rainbow trout and its role in secondary adaptive immune responses to nasal vaccines

Abstract

The olfactory organ of all vertebrates is constantly exposed to pathogens. The nasal mucosa is therefore equipped with a local immune system that protects the host from infection. In teleost fish, we previously described the presence of a diffuse nasopharynx-associated lymphoid tissue (NALT) found in the olfactory lamellae. This diffuse NALT (d-NALT) consists of myeloid and lymphoid cells but lacks an organized structure. Rainbow trout d-NALT mounts quick innate immune responses as well as adaptive immune responses to nasal vaccines. Here we report the discovery of a novel lymphoid structure located in the inner epithelial lining of the nasal cavity, opposite to the tips of the olfactory lamellae, in rainbow trout. This lymphoid structure represents the first description of an organized NALT (O-NALT) in teleost fish. Rainbow trout O-NALT is rich in B and T lymphocytes at the steady state with a proportion of approximately 8:3:1 IgM+ B cells, CD8+ T cells and IgT+ cells, respectively. Using laser capture microdissection we show that compared to d-NALT, O-NALT is highly enriched in expression of CD4, CD8 and IgM but not IgT. Strikingly, O-NALT expresses 8-fold higher levels of activation-induced cytidine deaminase aidc mRNA compared to d-NALT. Following primary and secondary intranasal vaccination with a live attenuated viral vaccine against infectious hematopoietic necrosis (IHN), trout O-NALT was expanded with increased numbers of B and T cell lymphocytes. Our results indicate that teleost fish posses organized lymphoid structures in the nasal cavity that participate in the maturation of the adaptive immune response and that need to be considered as important players in the response to mucosal vaccines. This work was supported by USDA NIFA award # 2020-67015-31457