A teleost structural analogue to the avian bursa of Fabricius

Abstract

The bursa of Fabricius is a primary and secondary lymphoid organ considered exclusively present in birds, and studies of this structure have been vital to our current understanding of the adaptive immune system of vertebrates. In this study, we reveal substantial lymphoepithelial tissue in a previously undescribed bursa in Atlantic salmon (Salmo salar), situated caudal to the urogenital papilla of the cloaca and thus analogous to the anatomical placement of the bursa of Fabricius. We investigated three groups of Atlantic salmon at different maturational stages and characterized the structure by applying dissection, radiology, scanning electron microscopy and histological techniques, including immunohistochemistry and in situ hybridization. We found that the epithelial anlage of the salmon cloacal bursa developed into substantial lymphoepithelial tissue and subsequently regressed following sexual maturation. Such a dynamic development is also a key characteristic of the avian bursa. The presence of intraepithelial lymphocytes was concomitant with expression of the leukocyteattracting chemokine CCL19, indicative of lymphoid organ functions. We did not observe recombination or gene conversion in salmon bursal lymphocytes at any developmental stage, indicating the absence of primary lymphoid organ functions in contrast to the bursa of Fabricius. However, the possibility of the bursa to trap both enteric and environmental antigens, combined with the presence of several antigen-presenting cells residing within the lymphoepithelium, suggest the structure has secondary lymphoid organ functions. We present the discovery of a lymphoid organ in Atlantic salmon with striking topographical similarities to that of the bursa of Fabricius in birds. In addition, the age-dependent dynamics of its lymphoepithelium suggest functions related to the maturation processes of lymphocytes.

Anatomy of teleost fish immune structures and organs

“…However, these investigations promoted the identification of the “salmonid bursa” (Fig. 6 ) (Løken et al 2020 ). This structure appeared to be a mucosal bursa with topographical similarities to the avian bursa of Fabricius.…”

“…α/β T cells were much more abundant in the salmonid bursa lymphoepithelium compared with the ϒ/δ population, and here, also abundant IgD-positive cells were present. IgM-positive cells were not as numerous, and the amount of IgT-positive cells was negligible (Løken et al 2020 ). Clearly, this epithelium displays several surprises.…”

“…With respect to the nasopharynx-associated lymphoid tissue, a recent and excellent review has been published (Das and Salinas 2020 ), and this tissue will therefore only briefly be presented here. However, the recently discovered immune structures interbranchial lymphoid tissue (ILT) (Haugarvoll et al 2008 ) and the salmonid bursa (Løken et al 2020 ) need to be presented as lymphatic structures in the context of other fish immune organs and will therefore be of focus in this review.

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IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon

“…Furthermore, RNAscope [ 29 ] markedly improved the accuracy and sensitivity of in situ hybridizations, helping to overcome one of the main obstacles in fish immunology, i.e., the limited selection of specific antibodies targeting key cell markers. This technique enables visualization of transcripts of both immune and virus genes within Atlantic salmon tissues [ 30 , 31 , 32 , 33 ].…”

Control of enteric parasitic diseases of farmed gilthead sea bream: New insights into Enteromyxum leei (Myxozoa) and Enterospora nucleophila (Microsporidia) infections

“…Teleost head kidney is functionally related with the bone marrow in mammals (Kum & Sekkin, 2011;Zapata, 1979) or Bursa of Fabricius in birds (Løken et al, 2019), which are the main lymphohematopoietic organs, holding and differentiating blood cells precursors. At the same time, head kidney also serves as a secondary lymphoid organ, important in the induction and elaboration of the immune response.…”